Ribophorin II regulates breast tumor initiation and metastasis through the functional suppression of GSK3β

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Takahashi, Ryou U ^a   Takeshita, Fumitaka ^a   Honma, Kimi ^a   Ono, Masaya ^b   Kato, Kikuya ^c   Ochiya, Takahiro ^a  

^a Division of Cellular and Molecular Medicine   (United States)

^b NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^c OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; MEMBRANE PROTEIN; PROTEIN P53; RIBOPHORIN; TP53 PROTEIN, HUMAN;

BREAST TUMOR; DOWN REGULATION; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; SECONDARY; TUMOR CELL CULTURE; ARTICLE; METASTASIS;

BREAST NEOPLASMS; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MEMBRANE PROTEINS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84883156816     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep02474     Document Type: Article

References (49)

1. Shaulian, E., Zauberman, A., Ginsberg, D. & Oren, M. Identification of a minimal transforming domain of p53: negative dominance through abrogation of sequence-specific DNA binding. Mol Cell Biol 12, 5581-5592 (1992).
2. Kalo, E. et al. Mutant p53 attenuates the SMAD-dependent transforming growth factor beta1 (TGF-beta1) signaling pathway by repressing the expression of TGFbeta receptor type II. Mol Cell Biol 27, 8228-8242 (2007). (Pubitemid 350234236)
3. Muller, P. A. et al. Mutant p53 drives invasion by promoting integrin recycling. Cell 139, 1327-1341 (2009).
4. Song, H., Hollstein, M. & Xu, Y. p53 gain-of-function cancer mutants induce genetic instability by inactivating ATM. Nat Cell Biol 9, 573-580 (2007). (Pubitemid 46696539)
5. Adorno, M. et al. A Mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis. Cell 137, 87-98 (2009).
6. Li, D., Marchenko, N. D. & Moll, U. M. SAHA shows preferential cytotoxicity in mutant p53 cancer cells by destabilizing mutant p53 through inhibition of the HDAC6-Hsp90 chaperone axis. Cell Death Differ 18, 1904-1913 (2011).
7. Peng, Y., Chen, L., Li, C., Lu, W. & Chen, J. Inhibition of MDM2 by hsp90 contributes to mutant p53 stabilization. J Biol Chem 276, 40583-40590 (2001).
8. Trepel, J., Mollapour, M., Giaccone, G. & Neckers, L. Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 10, 537-549 (2010).
9. Powers, M. V., Clarke, P. A. Workman, P. Dual targeting of HSC70 and HSP72 inhibits HSP90 function and induces tumor-specific apoptosis. Cancer Cell 14, 250-262 (2008).
10. Yan, W. et al. Histone deacetylase inhibitors suppress mutant p53 transcription via histone deacetylase 8. Oncogene (2012).
11. Chang, C. J. et al. p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating miRNAs. Nat Cell Biol 13, 317-32 (2011).
12. Onder, T. T. et al. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 68, 3645-3654 (2008).
13. Oft, M., Akhurst, R. J.,Balmain, A.Metastasis is driven by sequential elevation of H-ras and Smad2 levels. Nat Cell Biol 4, 487-494 (2002). (Pubitemid 34752433)
14. Mani, S. A. et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715 (2008). (Pubitemid 351636299)
15. Bachelder, R. E., Yoon, S. O., Franci, C., de Herreros, A. G. & Mercurio, A. M. Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: implications for the epithelial-mesenchymal transition. J Cell Biol 168, 29-33 (2005). (Pubitemid 40111054)
16. Yook, J. I. et al. A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat Cell Biol 8, 1398-1406 (2006). (Pubitemid 44835115)
17. Li, Y. et al. Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin Cancer Res 16, 2580-2590 (2010).
18. Gupta, P. B. et al. Identification of selective inhibitors of cancer stem cells by highthroughput screening. Cell 138, 645-659 (2009).
19. Honma, K. et al. RPN2 gene confers docetaxel resistance in breast cancer. NatMed 14, 939-948 (2008).
20. Clevers, H. The cancer stem cell: premises, promises and challenges. NatMed 17, 313-319 (2011).
21. Yin, H. & Glass, J. The phenotypic radiation resistance of CD441/CD24(-or low) breast cancer cells is mediated through the enhanced activation ofATMsignaling. PloS one 6, e24080 (2011).
22. Calcagno, A. M. et al. Prolonged drug selection of breast cancer cells and enrichment of cancer stem cell characteristics. Journal of the National Cancer Institute 102, 1637-1652 (2010).
23. Al-Hajj, M.,Wicha, M. S., Benito-Hernandez, A., Morrison, S. J. & Clarke, M. F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100, 3983-3988 (2003). (Pubitemid 36418143)
24. Todaro, M. et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 1, 389-402 (2007). (Pubitemid 47506537)
25. Li, D. et al. Functional inactivation of endogenous MDM2 and CHIP by HSP90 causes aberrant stabilization of mutant p53 in human cancer cells. Mol Cancer Res 9, 577-588 (2011).
26. Muller, P., Hrstka, R., Coomber, D., Lane, D. P. & Vojtesek, B. Chaperonedependent stabilization and degradation of p53 mutants. Oncogene 27, 3371-3383 (2008). (Pubitemid 351769319)
27. Esser, C., Scheffner, M. & Hohfeld, J. The chaperone-associated ubiquitin ligase CHIP is able to target p53 for proteasomal degradation. J Biol Chem 280, 27443-27448 (2005). (Pubitemid 41040787)
28. Zhang, Y. et al. HSF1-dependent upregulation of Hsp70 by sulfhydryl-reactive inducers of the KEAP1/NRF2/ARE pathway. Chem Biol 18, 1355-1361 (2011).
29. Chiang, W. C., Ching, T. T., Lee, H. C., Mousigian, C. & Hsu, A. L. HSF-1 regulators DDL-1/2 link insulin-like signaling to heat-shock responses and modulation of longevity. Cell 148, 322-334 (2012).
30. Xavier, I. J. et al. Glycogen synthase kinase 3beta negatively regulates both DNAbinding and transcriptional activities of heat shock factor 1. J Biol Chem 275, 29147-29152 (2000).
31. Kim, D., Kim, S. H. & Li, G. C. Proteasome inhibitors MG132 and lactacystin hyperphosphorylate HSF1 and induce hsp70 and hsp27 expression. Biochem Biophys Res Commun 254, 264-268 (1999). (Pubitemid 29292051)
32. Liu, J. et al. p27 suppresses arsenite-induced Hsp27/Hsp70 expression through inhibiting JNK2/c-Jun-and HSF-1-dependent pathways. J Biol Chem 285, 26058-26065 (2010).
33. Wei, L. et al. Hsp27 participates in the maintenance of breast cancer stem cells through regulation of epithelial-mesenchymal transition and nuclear factorkappaB. Breast Cancer Res 13 (2011).
34. Ogretmen, B. & Safa, A. R. Expression of the mutated p53 tumor suppressor protein and its molecular and biochemical characterization in multidrug resistant MCF-7/Adr human breast cancer cells. Oncogene 14, 499-506 (1997). (Pubitemid 27087113)
35. Ono, M. et al. Prolyl 4-hydroxylation of alpha-fibrinogen: a novel protein modification revealed by plasma proteomics. J Biol Chem 284, 29041-29049 (2009).
36. Neal, C. L. & Yu, D. 14-3-3zeta as a prognostic marker and therapeutic target for cancer. Expert Opin Ther Targets 14, 1343-1354 (2010).
37. Danes, C. G. et al. 14-3-3 zeta down-regulates p53 in mammary epithelial cells and confers luminal filling. Cancer Res 68, 1760-1767 (2008). (Pubitemid 351416561)
38. Zambetti, G. P. & Levine, A. J. A comparison of the biological activities of wildtype and mutant p53. FASEB J 7, 855-865 (1993). (Pubitemid 23225541)
39. Cohen, P. & Frame, S. The renaissance of GSK3. Nat Rev Mol Cell Biol 2, 769-776 (2001). (Pubitemid 33679839)
40. Crimaudo, C., Hortsch, M., Gausepohl, H. & Meyer, D. I. Human ribophorins I and II: the primary structure and membrane topology of two highly conserved rough endoplasmic reticulum-specific glycoproteins. EMBO J 6, 75-82 (1987).
41. Wilson, C. M., Roebuck, Q. High, S. Ribophorin I regulates substrate delivery to the oligosaccharyltransferase core. Proc Natl Acad Sci USA 105, 9534-9539 (2008). (Pubitemid 352031336)
42. Ge, X., Loh, H. H. & Law, P. Y. mu-Opioid receptor cell surface expression is regulated by its direct interaction with Ribophorin I. Mol Pharmacol 75, 1307-1316 (2009).
43. Mehta, P. P. et al. Effective targeting of triple-negative breast cancer cells by PF-4942847, a novel oral inhibitor of Hsp 90. Clin Cancer Res 17, 5432-5442 (2011).
44. Yiu, C. C. et al. Down-regulation of heat-shock protein 70 (HSP-70) correlated with responsiveness to neoadjuvant aromatase inhibitor therapy in breast cancer patients. Anticancer Res 30, 3465-3472 (2010).
45. Li, Y. et al. Amplification of LAPTM4B and YWHAZ contributes to chemotherapy resistance and recurrence of breast cancer. Nat Med 16, 214-218 (2010).
46. Bug, M. & Dobbelstein, M. Anthracyclines induce the accumulation of mutant p53 through E2F1-dependent and-independent mechanisms. Oncogene (2011).
47. Cleator, S., Heller, W. Coombes, R. C. Triple-negative breast cancer: therapeutic options. Lancet Oncol 8, 235-244 (2007). (Pubitemid 46291713)
48. Gluz, O. et al. Triple-negative breast cancer-current status and future directions. Ann Oncol 20, 1913-1927 (2009).
49. Sun, B. et al. Identification of metastasis-related proteins and their clinical relevance to triple-negative human breast cancer. Clin Cancer Res 14, 7050-7059 (2008).