Argyrin A Reveals a Critical Role for the Tumor Suppressor Protein p27kip1 in Mediating Antitumor Activities in Response to Proteasome Inhibition

Cancer Cell

Volumn 14, Issue 1, 2008, Pages 23-35

  Nickeleit, Irina ^a   Zender, Steffen ^a   Sasse, Florenz ^b   Geffers, Robert ^b   Brandes, Gudrun ^a   Sörensen, Inga ^a   Steinmetz, Heinrich ^b   Kubicka, Stefan ^a   Carlomagno, Teresa ^c   Menche, Dirk ^b   Gütgemann, Ines ^d   Buer, Jan ^b   Gossler, Achim ^a   Manns, Michael P ^a   Kalesse, Markus ^b   Frank, Ronald ^b   Malek, Nisar P ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^d UNIVERSITY OF BONN   (Germany)

Author keywords

CELLCYCLE; CHEMBIO

Indexed keywords

ANTINEOPLASTIC AGENT; ARGYRIN A; BORTEZOMIB; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLINE; HYBRID PROTEIN; PEPTIDE; PHOSPHOTRANSFERASE; PROTEASOME; PROTEASOME INHIBITOR; SMALL INTERFERING RNA; TUMOR SUPPRESSOR PROTEIN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARCHANGIUM GEPHYRA; ARTICLE; CORRELATION ANALYSIS; ENZYME SUBSTRATE; HUMAN; MYXOCOCCALES; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN TARGETING; TUMOR CELL;

ARCHANGIUM GEPHYRA;

EID: 45849099115     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2008.05.016     Document Type: Article

References (37)

1. Adams J. The development of proteasome inhibitors as anticancer drugs. Cancer Cell 5 (2004) 417-421
2. Adams J. The proteasome: a suitable antineoplastic target. Nat. Rev. Cancer 4 (2004) 349-360
3. Ben-Izhak O., Lahav-Baratz S., Meretyk S., Ben-Eliezer S., Sabo E., Dirnfeld M., Cohen S., and Ciechanover A. Inverse relationship between Skp2 ubiquitin ligase and the cyclin dependent kinase inhibitor p27Kip1 in prostate cancer. J. Urol. 170 (2003) 241-245
4. Besson A., Gurian-West M., Schmidt A., Hall A., and Roberts J.M. p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev. 18 (2004) 862-876
5. Besson A., Hwang H.C., Cicero S., Donovan S.L., Gurian-West M., Johnson D., Clurman B.E., Dyer M.A., and Roberts J.M. Discovery of an oncogenic activity in p27Kip1 that causes stem cell expansion and a multiple tumor phenotype. Genes Dev. 21 (2007) 1731-1746
6. Crawford L.J., Walker B., Ovaa H., Chauhan D., Anderson K.C., Morris T.C., and Irvine A.E. Comparative selectivity and specificity of the proteasome inhibitors BzLLLCOCHO, PS-341, and MG-132. Cancer Res. 66 (2006) 6379-6386
7. Goukassian D., Diez-Juan A., Asahara T., Schratzberger P., Silver M., Murayama T., Isner J.M., and Andres V. Overexpression of p27(Kip1) by doxycycline-regulated adenoviral vectors inhibits endothelial cell proliferation and migration and impairs angiogenesis. FASEB J. 15 (2001) 1877-1885
8. Katayose Y., Kim M., Rakkar A.N., Li Z., Cowan K.H., and Seth P. Promoting apoptosis: a novel activity associated with the cyclin-dependent kinase inhibitor p27. Cancer Res. 57 (1997) 5441-5445
9. Katner A.L., Hoang Q.B., Gootam P., Jaruga E., Ma Q., Gnarra J., and Rayford W. Induction of cell cycle arrest and apoptosis in human prostate carcinoma cells by a recombinant adenovirus expressing p27(Kip1). Prostate 53 (2002) 77-87
10. Kossatz U., Vervoorts J., Nickeleit I., Sundberg H.A., Arthur J.S., Manns M.P., and Malek N.P. C-terminal phosphorylation controls the stability and function of p27kip1. EMBO J. 25 (2006) 5159-5170
11. Lamb J., Crawford E.D., Peck D., Modell J.W., Blat I.C., Wrobel M.J., Lerner J., Brunet J.P., Subramanian A., Ross K.N., et al. The Connectivity Map: using gene-expression signatures to connect small molecules, genes, and disease. Science 313 (2006) 1929-1935
12. Lenferink A.E., Simpson J.F., Shawver L.K., Coffey R.J., Forbes J.T., and Arteaga C.L. Blockade of the epidermal growth factor receptor tyrosine kinase suppresses tumorigenesis in MMTV/Neu + MMTV/TGF-alpha bigenic mice. Proc. Natl. Acad. Sci. USA 97 (2000) 9609-9614
13. Leung T., Chen X.Q., Manser E., and Lim L. The p160 RhoA-binding kinase ROK alpha is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol. 16 (1996) 5313-5327
14. Lightcap E.S., McCormack T.A., Pien C.S., Chau V., Adams J., and Elliott P.J. Proteasome inhibition measurements: clinical application. Clin. Chem. 46 (2000) 673-683
15. Maffucci T., Piccolo E., Cumashi A., Iezzi M., Riley A.M., Saiardi A., Godage H.Y., Rossi C., Broggini M., Iacobelli S., et al. Inhibition of the phosphatidylinositol 3-kinase/Akt pathway by inositol pentakisphosphate results in antiangiogenic and antitumor effects. Cancer Res. 65 (2005) 8339-8349
16. Malek N.P., Sundberg H., McGrew S., Nakayama K., Kyriakides T.R., and Roberts J.M. A mouse knock-in model exposes sequential proteolytic pathways that regulate p27Kip1 in G1 and S phase. Nature 413 (2001) 323-327
17. Montagnoli A., Fiore F., Eytan E., Carrano A.C., Draetta G.F., Hershko A., and Pagano M. Ubiquitination of p27 is regulated by Cdk-dependent phosphorylation and trimeric complex formation. Genes Dev. 13 (1999) 1181-1189
18. Nguyen L., Besson A., Heng J.I., Schuurmans C., Teboul L., Parras C., Philpott A., Roberts J.M., and Guillemot F. p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev. 20 (2006) 1511-1524
19. Nikiforov M.A., Riblett M., Tang W.H., Gratchouck V., Zhuang D., Fernandez Y., Verhaegen M., Varambally S., Chinnaiyan A.M., Jakubowiak A.J., and Soengas M.S. Tumor cell-selective regulation of NOXA by c-MYC in response to proteasome inhibition. Proc. Natl. Acad. Sci. USA 104 (2007) 19488-19493
20. Obeng E.A., Carlson L.M., Gutman D.M., Harrington Jr. W.J., Lee K.P., and Boise L.H. Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells. Blood 107 (2006) 4907-4916
21. Osoegawa A., Yoshino I., Tanaka S., Sugio K., Kameyama T., Yamaguchi M., and Maehara Y. Regulation of p27 by S-phase kinase-associated protein 2 is associated with aggressiveness in non-small-cell lung cancer. J. Clin. Oncol. 22 (2004) 4165-4173
22. Pfoertner S., Jeron A., Probst-Kepper M., Guzman C.A., Hansen W., Westendorf A.M., Toepfer T., Schrader A.J., Franzke A., Buer J., and Geffers R. Signatures of human regulatory T cells: an encounter with old friends and new players. Genome Biol. 7 (2006) R54
23. Philipp-Staheli J., Payne S.R., and Kemp C.J. p27(Kip1): regulation and function of a haploinsufficient tumor suppressor and its misregulation in cancer. Exp. Cell Res. 264 (2001) 148-168
24. Porter P.L., Barlow W.E., Yeh I.T., Lin M.G., Yuan X.P., Donato E., Sledge G.W., Shapiro C.L., Ingle J.N., Haskell C.M., et al. p27(Kip1) and cyclin E expression and breast cancer survival after treatment with adjuvant chemotherapy. J. Natl. Cancer Inst. 98 (2006) 1723-1731
25. Read M.A., Neish A.S., Luscinskas F.W., Palombella V.J., Maniatis T., and Collins T. The proteasome pathway is required for cytokine-induced endothelial-leukocyte adhesion molecule expression. Immunity 2 (1995) 493-506
26. Reichenbach H., and Höfle G. Myxobacteria as producers of secondary metabolites. In: Grabley S., and Thieriecke R. (Eds). Drug Discovery from Nature (1999), Springer Verlag, Berlin 149-179
27. Ridley A.J., and Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70 (1992) 389-399
28. Roccaro A.M., Hideshima T., Raje N., Kumar S., Ishitsuka K., Yasui H., Shiraishi N., Ribatti D., Nico B., Vacca A., et al. Bortezomib mediates antiangiogenesis in multiple myeloma via direct and indirect effects on endothelial cells. Cancer Res. 66 (2006) 184-191
29. Sasse F., Steinmetz H., Schupp T., Petersen F., Memmert K., Hofmann H., Heusser C., Brinkmann V., von Matt P., Hofle G., and Reichenbach H. Argyrins, immunosuppressive cyclic peptides from myxobacteria. I. Production, isolation, physico-chemical and biological properties. J. Antibiot. (Tokyo) 55 (2002) 543-551
30. Sutterluty H., Chatelain E., Marti A., Wirbelauer C., Senften M., Muller U., and Krek W. p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat. Cell Biol. 1 (1999) 207-214
31. Suzuki Y., Nakabayashi Y., and Takahashi R. Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death. Proc. Natl. Acad. Sci. USA 98 (2001) 8662-8667
32. Timmerbeul I., Garrett-Engele C.M., Kossatz U., Chen X., Firpo E., Grunwald V., Kamino K., Wilkens L., Lehmann U., Buer J., et al. Testing the importance of p27 degradation by the SCFskp2 pathway in murine models of lung and colon cancer. Proc. Natl. Acad. Sci. USA 103 (2006) 14009-14014
33. Tozer G.M., Kanthou C., and Baguley B.C. Disrupting tumour blood vessels. Nat. Rev. Cancer 5 (2005) 423-435
34. Vernon A.E., and Philpott A. A single cdk inhibitor, p27Xic1, functions beyond cell cycle regulation to promote muscle differentiation in Xenopus. Development 130 (2003) 71-83
35. Vlachos P., Nyman U., Hajji N., and Joseph B. The cell cycle inhibitor p57(Kip2) promotes cell death via the mitochondrial apoptotic pathway. Cell Death Differ. 14 (2007) 1497-1507
36. Wang X., Gorospe M., Huang Y., and Holbrook N.J. p27Kip1 overexpression causes apoptotic death of mammalian cells. Oncogene 15 (1997) 2991-2997
37. Zhang Q., Tian L., Mansouri A., Korapati A.L., Johnson T.J., and Claret F.X. Inducible expression of a degradation-resistant form of p27Kip1 causes growth arrest and apoptosis in breast cancer cells. FEBS Lett. 579 (2005) 3932-3940