Cancer Treatment Reviews
Volume 29 , Pages 49-57 , May 2003

Therapeutic anti-cancer targets upstream of the proteasome

  • Grzegorz Nalepa

      Affiliations

    • Program in Cellular and Molecular Biology, Baylor College of Medicine, Houston, TX, USA
  • ,
  • J Wade Harper

      Affiliations

    • Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, TX, USA
    • Corresponding Author InformationCorrespondence to: J. Wade Harper, PhD, Department of Biochemistry and Molecular Biology, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA. Tel.: 1-713-798-6993; fax: 1-713-796-9438

References 

  1. Hershko A, Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 1998;67:425–479
  2. Koepp DM, Harper JW, Elledge SJ. How the cyclin became a cyclin: regulated proteolysis in the cell cycle. Cell. 1999;97(4):431–434
  3. Hicke L. Protein regulation by monoubiquitin. Nat. Rev. Mol. Cell Biol. 2001;2(3):195–201
  4. Richardson PG, Barlogie B, Berenson J, et al. Phase II study of the proteasome inhibitor PS-341 in multiple myeloma patients (Pts) with relapsed/refractory disease: results from Cohort1 analysis. Proceedings of the American Society of Clinical Oncology – 38th Annual Meeting 2002; 21: 11a
  5. Orlowski RZ, Hall M, Voorhees P, et al.  Phase I study of the proteasome inhibitor bortezomib (PS-341, Velcade) in combination with pegylated liposomal doxorubicin (doxil) in patients with refractory hematologic malignancies. Blood. 2002;100(11):105a
  6. Aghajanian C, Soignet S, Dizon DS, et al.  A phase I trial of the novel proteasome inhibitor PS341 in advanced solid tumor malignancies. Clin. Cancer Res. 2002;8(8):2505–2511
  7. Adams J. Development of the proteasome inhibitor PS-341. Oncologist. 2002;7(1):9–16
  8. Gille H, Downward J. Multiple ras effector pathways contribute to G(1) cell cycle progression. J. Biol. Chem. 1999;274(31):22033–22040
  9. Sears R, Leone G, DeGregori J, Nevins JR. Ras enhances myc protein stability. Mol. Cell. 1999;3(2):169–179
  10. Sears R, Nuckolls F, Haura E, Taya Y, Tamai K, Nevins JR. Multiple ras-dependent phosphorylation pathways regulate myc protein stability. Genes Dev. 2000;14(19):2501–2514
  11. He TC, Sparks AB, Rago C, et al.  Identification of C-MYC as a target of the APC pathway. Science. 1998;281(5382):1509–1512
  12. Wang TC, Cardiff RD, Zukerberg L, Lees E, Arnold A, Schmidt EV. Mammary hyperplasia and carcinoma in MMTV-Cyclin D1 transgenic mice. Nature. 1994;369(6482):669–671
  13. Bortner DM, Rosenberg MP. Induction of mammary gland hyperplasia and carcinomas in transgenic mice expressing human cyclin E. Mol. Cell. Biol. 1997;17(1):453–459
  14. Sherr CJ. Cancer cell cycles. Science. 1996;274(5293):1672–1677
  15. Keyomarsi K, Tucker SL, Buchholz TA, et al.  Cyclin E and survival in patients with breast cancer. N. Engl. J. Med. 2002;347(20):1566–1575
  16. Harper JW, Elledge SJ. Cdk inhibitors in development and cancer. Curr. Opin. Genet. Dev. 1996;6(1):56–64
  17. Porter PL, Malone KE, Heagerty PJ, et al.  Expression of cell-cycle regulators P27Kip1 and cyclin E, alone and in combination, correlate with survival in young breast cancer patients. Nat. Med. 1997;3(2):222–225
  18. Loda M, Cukor B, Tam SW, et al.  Increased proteasome-dependent degradation of the cyclin-dependent kinase inhibitor P27 in aggressive colorectal carcinomas. Nat. Med. 1997;3(2):231–234
  19. Catzavelos C, Bhattacharya N, Ung YC, et al.  Decreased levels of the cell-cycle inhibitor P27Kip1 protein: prognostic implications in primary breast cancer. Nat. Med. 1997;3(2):227–230
  20. Chiarle R, Pagano M, Inghirami G. The cyclin dependent kinase inhibitor P27 and its prognostic role in breast cancer. Breast Cancer Res. 2001;3(2):91–94
  21. Di Cristofano A, De Acetis M, Koff A, Cordon-Cardo C, Pandolfi PP. PTEN and P27KIP1 cooperate in prostate cancer tumor suppression in the mouse. Nat. Genet. 2001;27(2):222–224
  22. Zheng N, Schulman BA, Song L, et al.  Structure of the Cul1-Rbx1-Skp1-F BoxSkp2 SCF ubiquitin ligase complex. Nature. 2002;416(6882):703–709
  23. Strohmaier H, Spruck CH, Kaiser P, Won KA, Sangfelt O, Reed SI. Human F-box protein HCdc4 targets cyclin E for proteolysis and is mutated in a breast cancer cell line. Nature. 2001;413(6853):316–322
  24. Koepp DM, Schaefer LK, Ye X, et al.  Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science. 2001;294(5540):173–177
  25. Moberg KH, Bell DW, Wahrer DC, Haber DA, Hariharan IK. Archipelago regulates cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature. 2001;413(6853):311–316
  26. Carrano AC, Eytan E, Hershko A, Pagano M. SKP2 Is required for ubiquitin-mediated degradation of the CDK inhibitor P27. Nat. Cell Biol. 1999;1(4):193–199
  27. Tedesco D, Lukas J, Reed SI. The PRb-related protein P130 is regulated by phosphorylation-dependent proteolysis via the protein–ubiquitin ligase SCF(Skp2. Genes Dev. 2002;16(22):2946–2957
  28. Gstaiger M, Jordan R, Lim M, et al.  Skp2 is oncogenic and overexpressed in human cancers. Proc. Natl. Acad. Sci. USA. 2001;98(9):5043–5048
  29. Signoretti S, Di Marcotullio L, Richardson A, et al.  Oncogenic role of the ubiquitin ligase subunit Skp2 in human breast cancer. J. Clin. Invest. 2002;110(5):633–641
  30. Hershko D, Bornstein G, Ben Izhak O, et al.  Inverse relation between levels of P27(Kip1) and of its ubiquitin ligase subunit Skp2 in colorectal carcinomas. Cancer. 2001;91(9):1745–1751
  31. Chiarle R, Fan Y, Piva R, et al.  S-phase kinase-associated protein 2 expression in non-Hodgkin’s lymphoma inversely correlates with P27 expression and defines cells in S phase. Am. J. Pathol. 2002;160(4):1457–1466
  32. Masuda TA, Inoue H, Sonoda H, et al.  Clinical and biological significance of S-phase kinase-associated protein 2 (Skp2) gene expression in gastric carcinoma: modulation of malignant phenotype by Skp2 overexpression, possibly via P27 proteolysis. Cancer Res. 2002;62(13):3819–3825
  33. Yokoi S, Yasui K, Saito-Ohara F, et al.  A novel target gene, SKP2, within the 5p13 amplicon that is frequently detected in small cell lung cancers. Am. J. Pathol. 2002;161(1):207–216
  34. Schiffer D, Cavalla P, Fiano V, Ghimenti C, Piva R. Inverse relationship between P27/Kip.1 and the F-box protein Skp2 in human astrocytic gliomas by immunohistochemistry and Western blot. Neurosci. Lett. 2002;328(2):125–128
  35. Lim MS, Adamson A, Lin Z, et al.  Expression of Skp2, a P27(Kip1) ubiquitin ligase, in malignant lymphoma: correlation with P27(Kip1) and proliferation index. Blood. 2002;100(8):2950–2956
  36. Yang G, Ayala G, Marzo AD, et al.  Elevated Skp2 protein expression in human prostate cancer: association with loss of the cyclin-dependent kinase inhibitor P27 and PTEN and with reduced recurrence-free survival. Clin. Cancer Res. 2002;8(11):3419–3426
  37. Mamillapalli R, Gavrilova N, Mihaylova VT, et al.  PTEN regulates the ubiquitin-dependent degradation of the CDK inhibitor P27(KIP1) through the ubiquitin E3 ligase SCF(SKP2. Curr. Biol. 2001;11(4):263–267
  38. Coats S, Whyte P, Fero ML, et al.  A new pathway for mitogen-dependent Cdk2 regulation uncovered in P27(Kip1)-deficient cells. Curr. Biol. 1999;9(4):163–173
  39. Lane DP, Lain S. Therapeutic exploitation of the P53 pathway. Trends Mol. Med. 2002;8(4 Suppl):S38–S42
  40. Balint EE, Vousden KH. Activation and activities of the P53 tumour suppressor protein. Br. J. Cancer. 2001;85(12):1813–1823
  41. Prasad G, Wang H, Agrawal S, Zhang R. Antisense anti-MDM2 oligonucleotides as a novel approach to the treatment of glioblastoma multiforme. Anticancer Res. 2002;22(1A):107–116
  42. Bottger V, Bottger A, Howard SF, et al.  Identification of novel Mdm2 binding peptides by phage display. Oncogene. 1996;13(10):2141–2147
  43. Bottger A, Bottger V, Sparks A, Liu WL, Howard SF, Lane DP. Design of a synthetic Mdm2-binding mini protein that activates the P53 response in vivo. Curr. Biol. 1997;7(11):860–869
  44. Inoue S, Orimo A, Hosoi T, et al.  Genomic binding-site cloning reveals an estrogen-responsive gene that encodes a RING finger protein. Proc. Natl. Acad. Sci. USA. 1993;90(23):11117–11121
  45. Ikeda K, Orimo A, Higashi Y, Muramatsu M, Inoue S. Efp as a primary estrogen-responsive gene in human breast cancer. FEBS Lett. 2000;472(1):9–13
  46. Thomson SD, Ali S, Pickles L, et al.  Analysis of estrogen-responsive finger protein expression in benign and malignant human breast. Int. J. Cancer. 2001;91(2):152–158
  47. Urano T, Saito T, Tsukui T, et al.  Efp targets 14-3-3σ for proteolysis and promotes breast tumour growth. Nature. 2002;417(6891):871–875
  48. Hermeking H, Lengauer C, Polyak K, et al.  14-3-3σ is a P53-regulated inhibitor of G2/M progression. Mol. Cell. 1997;1(1):3–11
  49. Chan TA, Hermeking H, Lengauer C, Kinzler KW, Vogelstein B. 14-3-3σ is required to prevent mitotic catastrophe after DNA damage. Nature. 1999;401(6753):616–620
  50. Deshaies RJ. SCF and cullin/ring H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol. 1999;15:435–467
  51. Wu K, Chen A, Pan ZQ. Conjugation of Nedd8 to CUL1 enhances the ability of the ROC1-CUL1 complex to promote ubiquitin polymerization. J. Biol. Chem. 2000;275(41):32317–32324
  52. Tanaka K, Suzuki T, Chiba T. The ligation systems for ubiquitin and ubiquitin-like proteins. Mol. Cell. 1998;8(5):503–512
  53. Lyapina S, Cope G, Shevchenko A, et al.  Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science. 2001;292(5520):1382–1385
  54. Cope GA, Suh GS, Aravind L, et al.  Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science. 2002;298(5593):608–611
  55. Verma R, Aravind L, Oania R, et al.  Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science. 2002;298(5593):611–615

PII: S0305-7372(03)00083-5

doi: 10.1016/S0305-7372(03)00083-5

Cancer Treatment Reviews
Volume 29 , Pages 49-57 , May 2003