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Expert Opinion on Therapeutic Patents Volume 10, 2000 - Issue 2
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Review

Targeting hyperproliferative disorders with cyclin dependent kinase inhibitors

Gustavo R Rosania Cellomics, Inc., 635 William Pitt Way, Pittsburgh, PA 15238, USA. [email protected]
&
Young-Tae Chang Cellomics, Inc., 635 William Pitt Way, Pittsburgh, PA 15238, USA. [email protected]
Pages 215-230 | Published online: 25 Feb 2005

Bibliography

  • CLURMAN BE, ROBERTS JM, GROUDINE M: Deregulation of cell cycle control in hematologic malignancies. Curr. Op. Hematol. (1996) 3:315–320.
  • CLURMAN BE, ROBERTS JM: Cell cycle and cancer. J. Natl. Cancer Inst. (1995) 87:1499–1501
  • STRAUSS M, LUKAS J, BARTEK J: Unrestricted cell cycling and cancer. Nature Med. (1995) 1:1245–1246.
  • HUNG DT, JAMISON TF, SCHREIBER SL: Understandingand controlling the cell cycle with natural products. Chem. Biol. (1996) 3:623–639.
  • BRAUN-DULLAEUS RC, MANN MJ, DZAU VJ: Cell cycleprogression: new therapeutic target for vascular proliferative disease. Circulation (1998) 98:82–89.
  • PIPPIN JW, QU Q, MEIJER L et al.: Direct in vivo inhibi-tion of the nuclear cell cycle cascade in experimental mesangial proliferative glomerulonephritis with Roscovitine, a novel cyclin-dependent kinase antago-nist. J. Clinical Invest. (1997) 100:2512–2520.
  • LI JM, BROOKS G: Cell cycle regulatory molecules(cyclins, cyclin-dependent kinases and cyclin-dependent kinase inhibitors) and the cardiovascular system; potential targets for therapy? Eur. Heart J. (1999) 20:406–420.
  • ISOBE M, SUZUKI J, MORISHITA R et al.: Downregulationof endothelin expression in allograft coronary arteries after gene therapy targeting Cdk2 kinase. Transp. Proc. (1998) 30:1007–1008.
  • FAHRAEUS R, FISCHER P, KRAUSZ E et al.: Newapproaches to cancer therapies. J. Pathology (1999) 187:138–46.
  • WEINBERG RA: The retinoblastoma protein and cellcycle control. Cell (1995) 81:323–330.
  • PLANAS-SILVA MD, WEINBERG RA: The restriction pointand control of cell proliferation. Curr. Opin. Cell Biol. (1997) 9:768–912.
  • WANG MB, BILLINGS KR, VENKATESAN N et al.: Inhibi-tion of cell proliferation in head and neck squamous cell carcinoma cell lines with antisense cyclinDl. Otolaryngology - Head Neck Sur. (1998) 119:593–599.
  • •Describes effects of antisense cyclin DI in cancer cell lines.
  • HIRST M, KOBOR MS, KURIAKOSE N et al.: GAL4 isregulated by the RNA polymerase II holoenzyme-associated cyclin-dependent protein kinase SRB10/CDK8. Mol. Cell (1999) 3:673–678.
  • LECLERC V, TASSAN JP, O'FARREL PH et al.: DrosophilaCdk8, a kinase partner of cyclin C that interacts with the large subunit of RNA polymerase II. Mol. Biol. Cell (1996) 7:505–513.
  • SHIEKHATTAR R, MERMELSTEIN F, FISHER RP et al.:Cdk-activating kinase complex is a component of human transcription factor TFIIH. Nature (1995) 374:283–7.
  • MAKELA TP, PARVIN JD, KIM J et al.: A kinase-deficienttranscription factor TFIIH is functional in basal and activated transcription. Proc. Natl. Acad. Sci. USA (1995) 92:5174–5178.
  • PIGINO G, PAGLINI G, ULLOA L et al.: Analysis of theexpression, distribution and function of cyclin dependent kinase 5 (cdk5) in developing cerebellar macroneurons. J. Cell Science (1997) 110:257–270.
  • NIKOLIC M, DUDEK H, KWON YT et al.: The cdk5/p35kinase is essential for neurite outgrowth during neuronal differentiation. Genes Develop. (1996) 10:816–826.
  • MANCEBO HS, LEE G, FLYGARE J et al. pTEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev. (1997) 11, 2633–2644
  • HANNON GJ, BEACH D: p151NK4B is a potential effector of TGF-beta-induced cell cycle arrest. Nature (1994) 371:257–261.
  • POLYAK K, KATO JY, SOLOMON MJ et al.: p27Kipl,a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Devel (1994) 8:9–22.
  • BROWN JP, WET W, SEDIVY JM: Bypass of senescence after disruption of p21CIP1/WAFlgene in normal diploid human fibroblasts. Science (1997) 291:831–834.
  • KATO JY, MATSUOKA M, POLYAK K et al.: Cyclic AMP-induced G1 phase arrest mediated by an inhibitor (p27Kipl) of cyclin-dependent kinase 4 activation. Cell (1994) 79:487–496.
  • POLYAK K, LEE, MH, ERDJUMENT-BROMAGE H et al: Cloning of p27Kipl, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell (1994) 78:59–66.
  • SHERR CJ, ROBERTS JM: CDK inhibitors: positive and negative regulators of Gl-phase progression. Genes Devel (1999) 13:1501–1512.
  • EL DEIRY WS, TOKINO T, VELCULESCU VE et al.: WAF1, a potential mediator of p53 tumor suppression. Cell (1993) 75:817–825.
  • •Shows that WAF1 inhibits cell proliferation downstream of p53.
  • LADHA MH, LEE KY, UPTON TM et al: Regulation of exit from quiescence by p27 and cyclin Di-CDK4. Mol. Biol. (1998) 18:6655–6615.
  • XIONG Y, HANNON GJ, ZHANG H et al.: p21 is a universal inhibitor of cyclin kinases. Nature (1993) 366:701–704.
  • HARPER JW, ELLEDGE SJ, KEYOMARSI K et al.: Inhibition of cyclin-dependent kinases by p21. Mol. Biol. Cell (1995) 6:387–400.
  • RIVARD N, L'ALLEMAIN G, BARTEK J et al.: Abrogation of p27Kipl by cDNA antisense suppresses quiescence (GO state) in fibroblasts. J. Biol. Chem. (1996) 271:18337–18341.
  • COATS S, FLANAGAN WM, NOURSE J et al.: Requirementof p27Kipl for restriction point control of the fibroblast cell cycle. Science (1996) 272:891–880.
  • YAN Y, FRISAEN J, LEE MH, MASSAGUE J et al.: Ablation ofthe CDK inhibitor p57kip2 results in increased apoptosis and delayed differentiation during mouse development. Genes Devel. (1997) 11:973–983.
  • KOH J, ENDERS GH, DYNLACHT BD et al.: Tumour-derived p16 alleles encoding proteins defective in cell-cycle inhibition. Nature (1995) 375:506–510.
  • GUAN KL, JENKINS CW, LI Y et al.: Growth suppressionby p18, a p161NK4/MTS1- and p141NK4B/MTS2-related CDK6 inhibitor, correlates with wild-type pRb function. Genes Develop. (1994) 8:2939–2952.
  • •Shows that p16 or p18 inhibit cell proliferation, upstream of Rb.
  • HIRAI H, ROUSSEL MF, KATO JY et al.: Novel INK4 proteins, p19 and p18, are specific inhibitors of the cyclin D-dependent kinases CDK4 and CDK6. Mol. Biol. (1995) 15:2672–2681.
  • CHAN FK, ZHANG J, CHENG L et al.: Identification of human and mouse p19, a novel CDK4 and CDK6 inhibitor with homology to p 16ink4. Mol. Cell. Biol. (1995) 15:2682–2688.
  • SERRANO M, HANNON GJ, BEACH D: A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature (1993) 366:704–707.
  • SERRRANO M, GOMEZ-LAHOZ E, DEPINHO RA et al.: Inhibition of ras-induced proliferation and cellular transformation by p161NK4. Science (1995) 267:249–252.
  • •Demonstrates the inhibition of cell proliferation by p16, downstream of ras.
  • LUKAS J, PARRY D, AAGAARD L et al.: Retinoblastoma-protein-dependent cell-cycle inhibition by the tumour suppressor p16. Nature (1995) 375:503–506.
  • DENG C, ZHANG P, HARPER JW et al.: Mice lacking p21C1P1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell (1995) 82:675–684.
  • GARNER-HAMRICK PA, FISHER C: Antisense phosphorothioate oligonucleotides specifically down-regulate cdc25B causing S-phase delay and persistent antiproliferative effects. Int. J. Cancer (1998) 76:720–728.
  • •Presents the potential use of phosphorothioate oligonucleo-tides in antisense treatments targeting cdc25B.
  • ZUO Z, DEAN NM, HONKANEN RE: Serine/threonine protein phosphatase Type 5 acts upstream of p53 to regulate the induction of p21 (WAF1/Cip 1) and mediate growth arrest. J. Biol. Chem. (1998) 273:12250–12258.
  • PARRY D, MAHONY D, WILLS K et al.: Cyclin D-CDKsubunit arrangement is dependent on the availability of competing INK4 and p21 class inhibitors. Mol. Biol. (1999) 19:1915–1783.
  • KAMB A, GRIUS NA, WEAVER-FELDHAUS J et al.: A cell cycle regulator potentially involved in genesis of many tumor types. Science (1994) 264:436–440.
  • OKAMOTO A, DEMETRICK DJ, SPILLARE EA et al.: Mutation and altered expression of p 1 OM in human cancer. Proc. Natl. Acad. Sci. USA (1994) 91:11045–11049.
  • CALDAS C, HAHN SA, DA COSTA LT et al.: Frequent somatic mutations and homozygous deletions of the p16 (MTS1) gene in pancreatic adenocarcinoma. Nature Gen. (1994) 8:27–32.
  • HUSSUSSIAN CJ, STRUEWING JP, GOLDSTEIN AM et al.: Germline p16 mutations in familial melanoma. Nature Gen. (1994) 8:15–21.
  • KEUM JS, KONG G, YANG SC et al.: Cyclin Di overexpres-sion is an indicator of poor prognosis in resectable non-small cell lung cancer. Br. J. Cancer (1999) 81:127–132.
  • OYAMA T, KASHIWABARA K, YOSHIMOTO K et al: Frequent overexpression of the cyclin Di oncogene in invasive lobular carcinoma of the breast. Cancer Res. (1998) 58:2876–2880.
  • HUNTER T, PINES J: Cyclins and cancer. II: Cyclin D and CDK inhibitors come of age. Cell (1994) 79:573–582.
  • JIN X, NGUYEN D, ZHANG W et al.: Cell cycle arrest and inhibition of tumor cell proliferation by the p16INK4 gene mediated by an adenovirus vector. Cancer Res. (1995) 55:3250–3253.
  • •Describes a gene therapy vector for CDK inhibitor delivery.
  • CHANG MW, BARR E, LU MM et al: Adenovirus mediated over-expression of the cyclin/cyclin-dependent kinase inhibitor p21 inhibits vascular smooth muscle cell proliferation and neointima formation in the rat carotid artery model of balloon angioplasty. J. Clin. Invest. (1995) 96:2265–2268.
  • •Highlights the potential of gene therapy with CDK inhibitors in the treatment of restenosis.
  • EASTHAM JA, HALL SJ, SEHGAL I et al: In vivo gene therapy with p53 or p21 adenovirus for prostate cancer. Cancer Res. (1995) 55:5151–5155.
  • •Describes the results of animal studies using CDK inhibitor gene therapy, for prostrate cancer.
  • TSAO YP, HUANG SJ, CHANG JL et al.: Adenovirus-mediated p21 ((WAF1/SDII/CIP1)) gene transfer induces apoptosis of human cervical cancercell lines. Virol (1999) 73:4983–4990.
  • SANDIG V, BRAND K, HERWIG S et al: Adenovirally transferred p16INK4/CDKN2 and p53 genes cooperate to induce apoptotic tumor cell death. Nature Med. (1997) 3:313–319.
  • •Describes the cooperative effect of combination gene therapy with p16 and p53.
  • COLAS P, COHEN B, JESSEN T et al: Genetic selection of peptide aptamers that recognize and inhibit cyclin-dependent kinase 2. Nature (1996) 380:548–550.
  • COHEN B, COLAS P, BRENT R.: An artificial cell cycle inhibitor isolated from a combinatorial library. Proc. Natl. Acad. Sci. USA (1998) 95:14272–14291.
  • •Explores the use of the two hybrid system for identifying unnatural CDK inhibitors.
  • BALL KL, LAIN S, FAHRAEUS R et al: Cell-cycle arrest and inhibition of Cdk4 activity by small peptides based on the carboxy-terminal domain of p21WAF1. Curr. (1997) 7:71–80.
  • •Demonstrates that peptide fragments of p21 can inhibit cell growth.
  • FAHRAEUS R, PARAMIO JM, BALL KL et al.: Inhibition of pRb phosphorylation and cell-cycle progression by a 20-residue peptide derived from p16CDKN2/INK4A. Curr. Biol. (1996) 6:84–91.
  • •Demonstrates that peptide fragments of p16 can inhibit cell growth.
  • DE LUCA A, MACLACHLAN TK, BAGELLA L et al.: A unique domain of pRb2/p130 acts as an inhibitor of CDK2 kinase activity. J. Biol. Chem. (1997) 272:20971–20974.
  • •Demonstrates that fragments of Rb -a CDK substrate- can antagonise CDK function and inhibit cell growth.
  • CHEN Y-NP, SHARMA SK, TAMSEY TM et al: Selective killing of transformed cells by cyclin/cyclin-dependent kinase 2 antagonists. Proc. Natl. Acad. Sci. USA (1999) 96:4325–4329.
  • •Links deregulated E2F function to the sensitisation of cancer cells to CDK inhibitors.
  • BANDARA LR, GIRLING R, LA THANGUE NB et al: Apoptosis induced in mammalian cells by small peptides that functionally antagonize the Rb-regulated E2F transcription factor. Nature Biotechnol. (1997) 15:896–901.
  • •Determines that apoptosis can be induced by peptides that antagonise E2F function.
  • SKOWYRA D, CRAIG KL, TYERS M et al: F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell (1997) 91:209–219.
  • BAI C, SEN P, HOFMANN K et al.: SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell (1996) 86:263–74.
  • TASSAN JP, JAQUENOUD M, FRY AM et al.: In vitro assembly of a functional human CDK7-cyclin H complex requires MAT1, a novel 36 kDa RING finger protein. EMBO J (1995) 14:5658–5617.
  • KIMURA Y, RUTHERFORD SL, MIYATA Y et al.: Cdc37 is a molecular chaperone with specific functions in signal transduction. Genes Devel (1997) 11: 1915-1785.
  • DAI K, KOBAYASHI K, BEACH D: Physical interaction of mammalian CDC37 with CDK4. J. Biol. Chem. (1996) 271:22030–22034.
  • GEBER MR, FARRELL A, DESHAIES RJ et al.: Cdc37 is required for association of the protein kinase Cdc28 with G1 and mitotic cyclins. Proc. Nati Acad. Sci. USA (1995) 92:4651–4655.
  • PAVLETICH NP: Mechanisms of cyclin-dependent kinase regulation: structures of CDKs, their cyclin activators and cip and INK4 inhibitors. J. Mol. Biol. (1999) 287:821–828.
  • •Reviews crystallographic studies of CDKs in four different inhibitory complexes.
  • RUSSO AA, TONG L, LEE J-0 et al.: Structural basis for inhibition of the cyclin dependent kinase CDK6 by the tumor suppressor pl 6INK4a. Nature (1998) 395:237–243.
  • ••Crystal structure of a CDK-CDK inhibitor complex.
  • SCHULZE-GAHMEN U, JUNG JU, KIM S-H: Crystal structure of a viral cyclin, a positive regulator of cyclin-dependent kinase 6. Structure (1999) 7:245–254.
  • ENDICOTT JA, NOBLE MEM: Structural principles in cellcycle control: beyond the CDKs. Structure (1998) 6:535–541.
  • GRAY NS, DETIVAUD L, DOERIG C et al: ATP-sitedirected inhibitors of cyclin-dependent kinases. Curr. Med. Chem. (1999) 6:859–875.
  • •Reviews the scientific literature surrounding ATP site-directed CDK inhibitors.
  • GRAY NS, WODICKA L, THUNNISSENE AWH et al.: Exploiting chemical libraries, structure, and genomics in the search for kinase inhibitors. Science (1998) 281:533–538.
  • ••Describes the genome-wide transcriptional changesinduced by a small molecule CDK inhibitor.
  • HAVLICEK L, HANUS J, VESELY J et al: Cytokinin-derived cyclin-dependent kinase inhibitors: synthesis and cdc2 inhibitory activity of olomoucine and related compounds. J. Med. Chem. (1997) 40:408–412.
  • •Describes the synthesis of the first purine-based CDK inhibitors.
  • MEIJER L, BORGNE A, MULNER O et al.: Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2, and cdk5. Eur. J. Biochem. (1997) 243:527–536.
  • •Compares the inhibitory effects of roscovitine on a variety of kinases.
  • SCHULZE-GAHMEN U, BRANDSEN J, JONES HD et al: Multiple modes of ligand recognition: crystal structures of cyclin-dependent protein kinase 2 in complex with ATP and two inhibitors, olomoucine and isopentenyladenine. Proteins (1995) 22:378–391.
  • ••Crystal structures of CDK complexes with small moleculeinhibitors.
  • BROOKS EE, GRAY NS, JOLY A et al.: CVT-313, a specific and potent inhibitor of CDK2 that prevents neointimal proliferation. J. Biol. Chem. (1997) 272(46):29207–29211.
  • •Presents applications of small molecule CDK inhibitors for the treatment of restenosis.
  • CHANG YT, GRAY NS, ROSANIA GR et al.: Synthesis and application of functionally diverse 2,6,9-trisubstituted purine libraries as CDK inhibitors. Chem. Biol. (1999) 6(6)361–375.
  • ••Describes the rational synthesis of a library of smallmolecule CDK inhibitors with an unusually broad spectrum of physiological activities.
  • ROSANIA GR, MERLIE J, GRAY NS et al.: A cyclin- dependent kinase inhibitor inducing cancer cell differentiation: biochemical identification using Xenopus egg extracts. Proc. Natl. Acad. Sci. USA (1999) 96:4797–4802.
  • •Identifies the target of a unique CDK inhibitor, using a biochemical depletion-reconstitution approach using Xenopus egg extracts.
  • DE AZEVEDO WF, JR., MUELLER-DIECKMANN HJ, SCHULTZ-GAHMAN U, WORLAND PJ, SAUSVILLE E, KIM SH: Structural basis for specificity and potency of a flavonoid inhibitor of human CDK2, a cell cycle kinase. Proc. Natl. Acad. Sci. USA (1996) 93(7):2735–2740.
  • •Crystal structure of flavopiridol in complex with CDK2.
  • SENDEROWICZ AM, HEADLEE D, STINSON SF et al.: Phase I trial of continuous infusion flavopiridol, a novel cyclin-dependent kinase inhibitor, in patients with refractory neoplasms. J. Clin. Oncol. (1998) 16:2986–2999.
  • ••Results of the Phase I clinical trial with flavopiridol.
  • CHIEN M, ASTUMIAN M, LIEBOWITZ D et al.: In vitro evaluation of flavopiridol, a novel cell cycle inhibitor, in bladder cancer. Cancer Chem other. Pharmacol. (1999) 44:81–87.
  • HOOIJBERG JH, BROXTERMAN HJ, SCHEFFER GL et al: Potent interaction of flavopiridol with MRP1. British J. Cancer (1999) 81:269–276.
  • BRUSSELBACK S, NETLEBECK DM, SEDLACEK H-H et al: Cell cycle-independent induction of apoptosis by the antitumor drug flavopiridol in endothelial cells. Int. J. Cancer (1998) 91:146–152.
  • MEIJER L: Chemical inhibitors of cyclin dependent kinases. Trends Cell Biol. (1998) 6:393–397.
  • •Reviews scientific literature surrounding small molecule CDK inhibitors.
  • ARBER N, DOKI Y, HAN EK et al.: Antisense to cyclin Di inhibits the growth and tumorigenicity of human colon cancer cells. Cancer Res. (1997) 57:1569–1574.
  • ZHOU P, JIANG W, ZHANG YJ et al.: Antisense to cyclin Di inhibits growth and reverses the transformed phenotype of human esophageal cancer cells. Oncogene (1995) 11:571–580.
  • ARBER N, DOKI Y, HAN EK et al.: Antisense to cyclin Di inhibits the growth and tumorigenicity of human colon cancer cells. Cancer Res. (1997) 57:1569–1574.
  • SKOTSKO M, WU L, ANDERSON WF et al.: Retroviral vector mediated gene transfer of antisense cyclin G1 inhibits proliferation of human osteogenic sarcoma cells. Cancer Res. (1995) 55:5493–5498.
  • SUZUKI J, ISOBE M, MORISHITA R et al.: Prevention of graft coronary arteriosclerosis by antisense cdk2 kinase oligonucleotide. Nature Med. (1997) 3:900–903.
  • ••Explores therapeutic applications of antisense CDK2inhibitors.
  • WU L, CHEN P, HWNAG et al.: RNA antisense abrogation of MAT1 induces G1 phase arrest and triggers apoptosis in aortic smooth muscle cells. J. Biol. Chem. 274:5564-5572.
  • WEINSTEIN JN, MYERS TG, O'CONNOR PM et al.: An information-intensive approach to the molecular pharmacology of cancer. Science (1997) 275:343–349.
  • ••Explores the use of pattern recognition algorithms to studythe effects of different anticancer compounds in relation to molecular markers differentially expressed in cancer cells.
  • SHI LM, FAN Y, MYERS TG et al.: Mining the NCI anticancer drug discovery databases: genetic function approximation for the QSAR study of anticancer ellipticine analogues. J. Chem. Info. Comp. Sci. (1998) 38:189–199.
  • WANG DG, FAN JB, SIAO CJ et al.: Large-scale identifica- tion, mapping, and genotyping of single-nucleotide polymorphisms in the human genome. Science (1998) 280:1091–1082.
  • GOLUB TR, SLONIM P, TAMAYO C et al.: Molecular classi- fication of cancer: class discovery and class prediction by gene expression monitoring. Science (1999) 286:531–537.
  • ••Describes classification of different tumour types based ongene expression patterns.
  • JAMES VM, BRAMSON N, DICKERSON S et al: Identifica-tion of inhibitors of cyclin dependent kinases. In: Book ofAbstracts, 218th ACS national Meeting. New Orleans, USA (22–26 August 1999). MEDI–314.
  • SEITZ SP, BENFIELD PA, BOYLAN J et al: Characteriza-tion of indenopyrazoles as inhibitors of cyclin-dependent kinases. In: Book of Abstracts, 218th ACS national Meeting. New Orleans, USA (22–26 August 1999). MEDI–316.
  • NOBLE MEM, ENDICOTT JA.: Chemical inhibitors ofcyclin-dependent kinases: insights into design from X-ray crystallographic studies. Pharmacol Ther. (1999) 82:269–278.
  • •Reviews the rational design of specific, small molecule CDK inhibitors.
  • WALDMAN T, ZHANG Y, DILLEHAY L et al.: Cell-cycle arrest versus cell death in cancer therapy. Nature Med. (1997) 3:1034–1036.
  • •Demonstrates that isogenic cell lines differing in p21 gene expression display differential sensitivity to anticancer compounds.

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