Prodigiosin down-regulates SKP2 to induce p27KIP1 stabilization and antiproliferation in human lung adenocarcinoma cells

British Journal of Pharmacology

Volumn 166, Issue 7, 2012, Pages 2095-2108

  Hsieh, Hsin Ying ^a   Shieh, Jeng Jer ^a,b   Chen, Chun Jung ^a,b   Pan, Mu Yun ^a   Yang, Shu Yi ^a   Lin, Shin Chang ^a   Chang, Jo Shu ^c,d,e   Lee, Alan Yueh Luen ^f   Chang, Chia Che ^a,e,g  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^c Department of Chemical Engineering ^*  (Taiwan)

^d Research Center for Energy Technology and Strategy   (Taiwan)

^e NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^f NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^g CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

AKT; antiproliferation; lung adenocarcinoma; p27KIP1; PKB; prodigiosin; SKP2

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; PRODIGIOSIN; S PHASE KINASE ASSOCIATED PROTEIN 2; TRANSCRIPTION FACTOR E2F1;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CARCINOMA CELL; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; TRANSCRIPTION INITIATION; UPREGULATION;

ANTINEOPLASTIC AGENTS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DOWN-REGULATION; HUMANS; PRODIGIOSIN; PROTO-ONCOGENE PROTEINS C-AKT; S-PHASE KINASE-ASSOCIATED PROTEINS;

EID: 84862215651     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.01921.x     Document Type: Article

References (46)

1. Agarwal A, Bumm TG, Corbin AS, O'Hare T, Loriaux M, VanDyke J, et al,. (2008). Absence of SKP2 expression attenuates BCR-ABL-induced myeloproliferative disease. Blood 112: 1960-1970.
2. Bashir T, Dorrello NV, Amador V, Guardavaccaro D, Pagano M, (2004). Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 428: 190-193.
3. Borriello A, Bencivenga D, Criscuolo M, Caldarelli I, Cucciolla V, Tramontano A, et al,. (2011). Targeting p27Kip1 protein: its relevance in the therapy of human cancer. Expert Opin Ther Targets 15: 677-693.
4. KIP1 through SKP2 in human leukemia cells. J Biol Chem 286: 9815-9825.
5. Cataldo VD, Gibbons DL, Pérez-Soler R, Quintás-Cardama A, (2011). Treatment of non-small-cell lung cancer with erlotinib or gefitinib. N Engl J Med 364: 947-955.
6. Chan CH, Lee SW, Wang J, Lin HK, (2010). Regulation of Skp2 expression and activity and its role in cancer progression. Scientificworldjournal 10: 1001-1015.
7. Chang CC, Chen WC, Ho TF, Wu HS, Wei YH, (2011). Development of natural anti-tumor drugs by microorganisms. J Biosci Bioeng 111: 501-511.
8. Chen JJ, Peck K, Hong TM, Yang SC, Sher YP, Shih JY, et al,. (2001). Global analysis of gene expression in invasion by a lung cancer model. Cancer Res 61: 5223-5230.
9. Chen JY, Wang MC, Hung W, (2009). Transcriptional activation of Skp2 by BCR-ABL in K562 chronic myeloid leukemia cells. Leuk Res 33: 1520-1524.
10. Skp2 results in p27- and Skp2-mediated cell cycle arrest and activation of autophagy. Blood 111: 4690-4699.
11. Chu IM, Hengst L, Slingerland JM, (2008). The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy. Nat Rev Cancer 8: 253-267.
12. Ecker K, Hengst L, (2009). Skp2: caught in the Akt. Nat Cell Biol 11: 377-379.
13. Frescas D, Pagano M, (2008). Deregulated proteolysis by the F-box proteins SKP2 and β-TrCP: tipping the scales of cancer. Nat Rev Cancer 8: 438-449.
14. Gao D, Inuzuka H, Tseng A, Chin RY, Toker A, Wei W, (2009). Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat Cell Biol 11: 397-408.
15. Ho TF, Peng YT, Chuang SM, Lin SC, Feng BL, Lu CH, et al,. (2009). Prodigiosin down-regulates survivin to facilitate paclitaxel sensitization in human breast carcinoma cell lines. Toxicol Appl Pharmacol 235: 253-260.
16. kip1 in E2-stimulated MCF-7 cells through down-regulation of the Skp2 protein. Endocrinology 149: 5972-5983.
17. Skp2 expression via the Sp1 sites in human prostate cancer cells. J Cell Physiol 209: 363-369.
18. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D, (2011). Global cancer statistics. CA Cancer J Clin 61: 69-90.
19. Lin HK, Wang G, Chen Z, Teruya-Feldstein J, Liu Y, Chan CH, et al,. (2009). Phosphorylation-dependent regulation of cytosolic localization and oncogenic function of Skp2 by Akt/PKB. Nat Cell Biol 11: 420-432.
20. Lin HK, Chen Z, Wang G, Nardella C, Lee SW, Chan CH, et al,. (2010). Skp2 targeting suppresses tumorigenesis by Arf-p53-independent cellular senescence. Nature 464: 374-379.
21. KIP1 up-regulation and nuclear translocation in association with cell growth inhibition and G1/S phase arrest in human non-small-cell lung cancer cell lines. Mol Pharmacol 72: 248-258.
22. Liu S, Yamauchi H, (2009). p27-associated G1 arrest induced by hinokitiol in human malignant melanoma cells is mediated via down-regulation of pRb, Skp2 ubiquitin ligase, and impairment of cdk2 function. Cancer Lett 286: 240-249.
23. Kip1 signaling axis. Cancer Res 68: 9015-9023.
24. Maemondo M, Inoue A, Kobayashi K, Sugawara S, Oizumi S, Isobe H, et al,. (2010). Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med 362: 2380-2388.
25. Kip1, polyploidy and centrosome overduplication. EMBO J 19: 2069-2081.
26. Nakayama K, Nagahama H, Minamishima YA, Miyake S, Ishida N, Hatakeyama S, et al,. (2004). Skp2-mediated degradation of p27 regulates progression into mitosis. Dev Cell 6: 661-672.
27. Niculescu AB III, Chen X, Smeets M, Hengst L, Prives C, Reed SI, (1998). Effects of p21(Cip1/Waf1) at both the G1/S and the G2/M cell cycle transitions: pRb is a critical determinant in blocking DNA replication and in preventing endoreduplication. Mol Cell Biol 18: 629-643.
28. Ohtani K, DeGregori J, Nevins JR, (1995). Regulation of the cyclin E gene by transcription factor E2F1. Proc Natl Acad Sci U S A 92: 12146-12150.
29. Pandey R, Chander R, Sainis KB, (2009). Prodigiosins as anti-cancer agents: living upto their name. Curr Pharm Des 15: 732-741.
30. Pang PH, Lin YH, LeeYH HHH, Hsu SP, Juan SH, (2008). Molecular mechanisms of p21 and p27 induction by 3-methylcholanthrene, an aryl-hydrocarbon receptor agonist, involved in antiproliferation of human umbilical vascular endothelial cells. J Cell Physiol 215: 161-171.
31. Pérez-Tomás R, Viñas M, (2010). New insights on the antitumoral properties of prodiginines. Curr Med Chem 17: 2222-2231.
32. Ramalingam SS, Owonikoko TK, Khuri FR, (2011). Lung Cancer: new biological insights and recent therapeutic advances. CA Cancer J Clin 61: 91-112.
33. Reichert M, Saur D, Hamacher R, Schmid RM, Schneider G, (2007). Phosphoinositide-3-kinase signaling controls S-phase kinase-associated protein 2 transcription via E2F1 in pancreatic ductal adenocarcinoma cells. Cancer Res 67: 4149-4156.
34. Sonoda H, Inoue H, Ogawa K, Utsunomiya T, Masuda TA, Mori M, (2006). Significance of skp2 expression in primary breast cancer. Clin Cancer Res 12: 1215-1220.
35. WAF1/CIP1 expression via transforming growth factor-beta receptor pathway. Biochem Pharmacol 4: 1340-1349.
36. Soto-Cerrato V, Viñals F, Lambert JR, Kelly JA, Pérez-Tomás R, (2007b). Prodigiosin induces the proapoptotic gene NAG-1 via glycogen synthase kinase-3β activity in human breast cancer cells. Mol Cancer Ther 6: 362-369.
37. Uddin S, Ahmed M, Bavi P, El-Sayed R, Al-Sanea N, AbdulJabbar A, et al,. (2008). Bortezomib (Velcade) induces p27Kip1 expression through S-phase kinase protein 2 degradation in colorectal cancer. Cancer Res 68: 3379-3388.
38. Uddin S, Ahmed M, Hussain AR, Jehan Z, Al-Dayel F, Munkarah A, et al,. (2009). Bortezomib-mediated expression of p27Kip1 through S-phase kinase protein 2 degradation in epithelial ovarian cancer. Lab Invest 89: 1115-1127.
39. +/- mice. Nat Genet 42: 83-88.
40. Kip1 nuclear localization and cyclin-dependent kinase inhibitory activity are regulated by glycogen synthase kinase-3 in human colon cancer cells. Cell Death Differ 15: 908-919.
41. Wei W, Ayad NG, Wan Y, Zhang GJ, Kirschner MW, Kaelin WG Jr, (2004). Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex. Nature 428: 194-198.
42. Williamson NR, Fineran PC, Leeper FJ, Salmond GP, (2006). The biosynthesis and regulation of bacterial prodiginines. Nat Rev Microbiol 4: 887-899.
43. Xu Y, Liu H, Chen J, Zhou Q, (2010). Acquired resistance of lung adenocarcinoma to EGFR-tyrosine kinase inhibitors gefitinib and erlotinib. Cancer Biol Ther 9: 572-582.
44. Yoshida T, Zhang G, Haura EB, (2010). Targeting epidermal growth factor receptor: central signaling kinase in lung cancer. Biochem Pharmacol 80: 613-623.
45. Zhang L, Wang C, (2006). F-box protein Skp2: a novel transcriptional target of E2F. Oncogene 25: 2615-2627.
46. Zuo T, Liu R, Zhang H, Chang X, Liu Y, Wang L, et al,. (2007). FOXP3 is a novel transcriptional repressor for the breast cancer oncogene SKP2. J Clin Invest 117: 3765-3773.