RSK1 protects P-glycoprotein/ABCB1 against ubiquitin-proteasomal degradation by downregulating the ubiquitin-conjugating enzyme E2 R1

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Katayama, Kazuhiro ^a   Fujiwara, Chiaki ^a   Noguchi, Kohji ^a   Sugimoto, Yoshikazu ^a  

^a KEIO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BORTEZOMIB; CDC34 PROTEIN, HUMAN; F BOX PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 3; MULTIDRUG RESISTANCE PROTEIN 1; PROTEASOME; PROTEASOME INHIBITOR; PROTEIN BINDING; PYRIDONE DERIVATIVE; PYRIMIDINONE DERIVATIVE; RIBOSOMAL PROTEIN S6 KINASE, 90KDA, POLYPEPTIDE 3; RPS6KA1 PROTEIN, HUMAN; S6 KINASE; TRAMETINIB; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME;

ANTAGONISTS AND INHIBITORS; DOWN REGULATION; DRUG EFFECT; DRUG RESISTANCE; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; PHOSPHORYLATION; RNA INTERFERENCE; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; ATP-BINDING CASSETTE, SUB-FAMILY B, MEMBER 1; BORTEZOMIB; CELL LINE, TUMOR; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; F-BOX PROTEINS; HEK293 CELLS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; PROTEIN BINDING; PYRIDONES; PYRIMIDINONES; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; RNA INTERFERENCE; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84994056620     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep36134     Document Type: Article

References (44)

1. Dean, M., Rzhetsky, A. & Allikmets, R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 11, 1156-1166 (2001).
2. Schinkel, A. H. & Jonker, J. W. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv. Drug Deliv. Rev. 64, 138-153 (2012).
3. Chen, Z. et al. Mammalian drug efflux transporters of the ATP binding cassette (ABC) family in multidrug resistance: A review of the past decade. Cancer Lett. 370, 153-164 (2016).
4. Kartner, N., Shales, M., Riordan, J. R. & Ling, V. Daunorubicin-resistant Chinese hamster ovary cells expressing multidrug resistance and a cell-surface P-glycoprotein. Cancer Res. 43, 4413-4419 (1983).
5. Hamada, H. & Tsuruo, T. Functional role for the 170-to 180-kDa glycoprotein specific to drug-resistant tumor cells as revealed by monoclonal antibodies. Proc. Natl. Acad. Sci. USA. 83, 7785-7789 (1986).
6. Mickisch, G. H., Pai, L. H., Gottesman, M. M. & Pastan, I. Monoclonal antibody MRK16 reverses the multidrug resistance of multidrug-resistant transgenic mice. Cancer Res. 52, 4427-4432 (1992).
7. Tanigawara, Y. et al. Transport of digoxin by human P-glycoprotein expressed in a porcine kidney epithelial cell line (LLC-PK1). J. Pharmacol. Exp. Ther. 263, 840-845 (1992).
8. Yamazaki, M., Suzuki, H. & Sugiyama, Y. Recent advances in carrier-mediated hepatic uptake and biliary excretion of xenobiotics. Pharm. Res. 13, 497-513 (1996).
9. Huisman, M. T., Smith, J. W. & Schinkel, A. H. Significance of P-glycoprotein for the pharmacology and clinical use of HIV protease inhibitors. AIDS 14, 237-242 (2000).
10. Gottesman, M. M., Hrycyna, C. A., Schoenlein, P. V., Germann, U. A. & Pastan, I. Genetic analysis of the multidrug transporters. Annu. Rev. Genet. 29, 607-649 (1995).
11. Gottesman, M. M., Fojo, T. & Bates, S. E. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer 2, 48-58 (2002).
12. Leslie, E. M., Deeley, R. G. & Cole, S. P. Multidrug resistance proteins: role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. 204, 216-237 (2005).
13. Katayama, K., Noguchi, K. & Sugimoto, Y. Regulations of P-glycoprotein/ABCB1/MDR1 in human cancer cells. New J. Sci. 2014, 476974 (2014).
14. Traverse, S. et al. Specific association of activated MAP kinase kinase kinase (Raf) with the plasma-membranes of Ras-transformed retinal cells. Oncogene 8, 3175-3181 (1993).
15. Chang, F. et al. Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors: potential targeting for therapeutic intervention. Leukemia 17, 1263-1293 (2003).
16. Nagata, D. et al. Transcriptional activation of the cyclin D1 gene is mediated by multiple cis-elements including SP1 sites and a cAMP-responsive element in vascular endothelial cells. J. Biol. Chem. 276, 662-669 (2001).
17. Fujita, S., Sato, S. & Tsuruo, T. Phosphorylation of p27Kip1 at threonine 198 by p90 ribosomal protein S6 kinases promotes its binding to 14-3-3 and cytoplasmic localization. J. Biol. Chem. 278, 49254-49260 (2003).
18. Wang, Z., Ge, L., Wang, M. & Carr, B. I. Phosphorylation regulates Myc expression via prolonged activation of the mitogen-activated protein kinase pathway. J. Cell. Physiol. 208, 133-140 (2006).
19. Chung, J., Uchida, E., Grammer, T. C. & Blenis, J. STAT3 serine phosphorylation by ERK-dependent and-independent pathways negatively modulates its tyrosine phosphorylation. Mol. Cell. Biol. 17, 6508-6516 (1997).
20. Lee, S. et al. RSK-mediated phosphorylation in the C/EBPβ leucine zipper regulates DNA binding, dimerization, and growth arrest activity. Mol. Cell. Biol. 30, 2621-2635 (2010).
21. Katayama, K., Yoshioka, S., Tsukahara, S., Mitsuhashi, J. & Sugimoto, Y. Inhibition of the mitogen-activated protein kinase pathway results in the down-regulation of P-glycoprotein. Mol. Cancer Ther. 6, 2092-2102 (2007).
22. Katayama, K., Noguchi, K. & Sugimoto, Y. FBXO15 regulates P-glycoprotein/ABCB1 expression through the ubiquitin-proteasome pathway in cancer cells. Cancer Sci. 104, 694-702 (2013).
23. Winston, J. T., Koepp, D. M., Zhu, C., Elledge, S. J. & Harper, J. W. A family of mammalian F-box proteins. Curr. Biol. 9, 1180-1182 (1999).
24. Jin, J. et al. Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev. 18, 2573-2580 (2004).
25. Tokuzawa, Y. et al. Fbx15 is a novel target of Oct3/4 but is dispensable for embryonic stem cell self-renewal and mouse development. Mol. Cell. Biol. 23, 2699-2708 (2003).
26. Sapkota, G. P. et al. Phosphorylation of the protein kinase mutated in Peutz-Jeghers cancer syndrome, LKB1/STK11, at Ser431 by p90RSK and cAMP-dependent protein kinase, but not its farnesylation at Cys433, is essential for LKB1 to suppress cell growth. J. Biol. Chem. 276, 19469-19482 (2001).
27. Eisenmann, K. M., VanBrocklin, M. W., Staffend, N. A., Kitchen, S. M. & Koo, H. M. Mitogen-activated protein kinase pathwaydependent tumor-specific survival signaling in melanoma cells through inactivation of the proapoptotic protein Bad. Cancer Res. 63, 8330-8337 (2003).
28. Katayama, K. et al. Revealing the fate of cell surface human P-glycoprotein (ABCB1): The lysosomal degradation pathway. Biochim. Biophys. Acta 1853, 2361-2370 (2015).
29. Katayama, K., Yamaguchi, M., Noguchi, K. & Sugimoto, Y. Protein phosphatase complex PP5/PPP2R3C dephosphorylates P-glycoprotein/ABCB1 and down-regulates the expression and function. Cancer Lett. 345, 124-131 (2014).
30. Wojtal, K. A., de Vries, E., Hoekstra, D. & van Ijzendoorn, S. C. Efficient trafficking of MDR1/P-glycoprotein to apical canalicular plasma membranes in HepG2 cells requires PKA-RIIalpha anchoring and glucosylceramide. Mol. Biol. Cell 17, 3638-3650 (2006).
31. Mattaloni, S. M. et al. AKAP350 is involved in the development of apical "canalicular" structures in hepatic cells HepG2. J. Cell. Physiol. 227, 160-171 (2012).
32. Hardy, S. P. et al. Protein kinase C-mediated phosphorylation of the human multidrug resistance P-glycoprotein regulates cell volume-activated chloride channels. EMBO J. 14, 68-75 (1995).
33. Michael, W. M. & Newport, J. Coupling of mitosis to the completion of S phase through Cdc34-mediated degradation of Wee1. Science 282, 1886-1889 (1998).
34. Pagano, M. et al. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 269, 682-685 (1995).
35. Katayama, K., Fujita, N. & Tsuruo, T. Akt/protein kinase B-dependent phosphorylation and inactivation of WEE1Hu promote cell cycle progression at G2/M transition. Mol. Cell Biol. 25, 5725-5737 (2005).
36. Fujita, N., Sato, S., Katayama, K. & Tsuruo, T. Akt-dependent phosphorylation of p27Kip1 promotes binding to 14-3-3 and cytoplasmic localization. J. Biol. Chem. 277, 28706-28713 (2002).
37. Neise, D. et al. The p90 ribosomal S6 kinase (RSK) inhibitor BI-D1870 prevents gamma irradiation-induced apoptosis and mediates senescence via RSK-and p53-independent accumulation of p21WAF1/CIP1. Cell Death Dis. 4, e859 (2013).
38. Chiu, C. F. et al. Antitumor effects of BI-D1870 on human oral squamous cell carcinoma. Cancer Chemother. Pharmacol. 73, 237-247 (2014).
39. Gilmartin, A. G. et al. GSK1120212 (JTP-74057) is an inhibitor of MEK activity and activation with favorable pharmacokinetic properties for sustained in vivo pathway inhibition. Clin. Cancer Res. 17, 989-1000 (2011).
40. Flaherty, K. T. et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N. Engl. J. Med. 367, 1694-1703 (2012).
41. Teicher, B. A., Ara, G., Herbst, R., Palombella, V. J. & Adams, J. The proteasome inhibitor PS-341 in cancer therapy. Clin. Cancer Res. 5, 2638-2645 (1999).
42. Hideshima, T., Richardson, P. & Chauhan, D. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res. 61, 3071-3076 (2001).
43. Richardson, P. G., Barlogie, B. & Berenson, J. A phase 2 study of bortezomib in relapsed, refractory myeloma. N. Engl. J. Med. 348, 2609-2617 (2003).
44. Flaherty, K. T., Robert, C. & Hersey, P. Improved survival with MEK inhibition in BRAF-mutated melanoma. N. Engl. J. Med. 367, 107-114 (2012).