Sgk1 enhances RANBP1 transcript levels and decreases taxol sensitivity in RKO colon carcinoma cells

Oncogene

Volumn 32, Issue 38, 2013, Pages 4572-4578

  Amato, R ^a   Scumaci, D ^a   D'antona, L ^a   Iuliano, R ^a,b   Menniti, M ^a   Di Sanzo, M ^a   Faniello, M C ^a   Colao, E ^b   Malatesta, P ^b   Zingone, A ^c   Agosti, V ^a   Costanzo, F S ^a   Mileo, A M ^d   Paggi, M G ^d   Lang, F ^e   Cuda, G ^a   Lavia, P ^f   Perrotti, N ^a,b  

^a UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^b Policlinico Mater Domini   (Italy)

^c NATIONAL CANCER INSTITUTE   (United States)

^d REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

mitotic microtubule stabilization; RANBP1; Sgk1; taxol sensitivity

Indexed keywords

GUANOSINE TRIPHOSPHATASE; NUCLEAR PROTEIN; PACLITAXEL; RAN BINDING PROTEIN 1; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; COLON CARCINOMA; CONTROLLED STUDY; DOWN REGULATION; DRUG SENSITIVITY; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; PRIORITY JOURNAL; PROMETAPHASE; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL ELECTROPHORESIS; UPREGULATION; WILD TYPE;

APOPTOSIS; CARCINOMA; CELL LINE, TUMOR; COLONIC NEOPLASMS; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMEDIATE-EARLY PROTEINS; NUCLEAR PROTEINS; PACLITAXEL; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEOMICS; RNA INTERFERENCE; SP1 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC;

EID: 84884591405     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.470     Document Type: Article

References (42)

1. Firestone GL, Giampaolo JR, O'Keeffe BA. Stimulus-dependent regulation of serum and glucocorticoid inducible protein kinase (Sgk) transcription, subcellular localization and enzymatic activity. Cell Physiol Biochem 2003; 13: 1-12.
2. Lang F, Böhmer C, Palmada M, Seebohm G, Strutz-Seebohm N, Vallon V. (Patho)physiological significance of the serum- and glucocorticoid-inducible kinase isoforms. Physiol Rev 2006; 86: 1151-1178.
3. Lang F, Perrotti N, Stournaras C. Colorectal carcinoma cells-regulation of survival and growth by Sgk1. Int J Biochem Cell Biol 2010; 42: 1571-1575.
4. Kobayashi T, Cohen P. Activation of serum- and glucocorticoid-regulated protein kinase by agonists that activate phosphatidylinositide 3-kinase is mediated by 3-phosphoinositidedependent protein kinase-1 (PDK1) and PDK2. Biochem J 1999; 339: 319-328.
5. Perrotti N, He RA, Phillips SA, Renfrew-Haft C, Taylor SI. Activation of serum and glucocorticoid- induced kinase (Sgk1) by cyclic AMP and Insulin. J Biol Chem 2001; 276: 9406-9412.
6. Hong F, Larrea MD, Doughty C, Kwiatkowski DJ, Squillace R, Slingerland JM. mTOR-raptor binds and activates Sgk1 to regulate p27 phosphorylation. Mol Cell 2008; 30: 701-711.
7. Faletti CJ, Perrotti N, Taylor SI, Blazer Yost BL. Sgk1: An essential convergence point for peptide and steroid hormone regulation of EnaC- mediated Na(+) transport. Am J Physiol 2001; 283: C494-500.
8. Chen SY, Bhargava A, Mastroberardino L, Meijer OC, Wang J, Buse P et al. Epithelial sodium channel regulated by aldosterone-induced protein sgk. Proc Natl Acad Sci USA 1999; 96: 2514-2519.
9. Alvarez De La Rosa D, Zhang P, Náray-Fejes-Tó th A, Fejes-Tó th G, Canessa CM. The serum and glucocorticoid kinase sgk increases the abundance of epithelial sodium channels in the plasma membrane of Xenopus oocytes. J Biol Chem 1999; 274: 37834-37839.
10. Liu D, Yang X, Songyang Z. Identification of CISK, a new member of the Sgk1 kinase family that promotes interleukin 3 dependent survival. Curr Biol 2000; 10: 1233-1236.
11. Leong ML, Maiyar AC, Kim B, O'Keefe BA, Firestone GL. Expression of the serumand glucocorticoid-inducible protein kinase, Sgk1, is a cell survival response to multiple types of environmental stress stimuli in mammary epithelial cells. J Biol Chem 2003; 278: 5871-5882.
12. Amato R, Menniti M, Agosti V, Boito R, Costa N, Bond HM et al. IL-2 signals through Sgk1 and inhibits proliferation and apoptosis in kidney cancer cells. J Mol Med 2007; 85: 707-721.
13. Amato R, D'Antona L, Porciatti G, Agosti V, Menniti M, Rinaldo C et al. Sgk1 activates MDM2-dependent p53 degradation and affects cell proliferation, survival, and differentiation. J Mol Med 2009; 87: 1221-1239.
14. Nasir O, Wang K, Föller M, Gu S, Bhandaru M, Ackermann TF et al. Relative resistance of Sgk1 knockout mice against chemical carcinogenesis. IUBMB Life 2009; 61: 768-776.
15. Wang K, Gu S, Nasir O, Foller M, Ackermann TF, Klingel K et al. Sgk1-dependent intestinal tumor growth in APC-deficient mice. Cell Physiol Biochem 2010; 25: 271-278.
16. Hu R, Lam W, Hsu CH, Cheng YC. UMP/CMPK is not the critical enzyme in the metabolism of pyrimidine ribonucleotide and activation of deoxycytidine analogs in human RKO cells. PLoS One 2011; 6: E19490.
17. Zhang Y, Bao YL, Yang MT, Wu Y, Yu CL, Huang YX et al. Activin A induces SLC5A8 expression through the Smad3 signaling pathway in human colon cancer RKO cells. Int J Biochem Cell Biol 2010; 42: 1964-1972.
18. Guarguaglini G, Renzi L, D'Ottavio F, Di Fiore B, Casenghi M, Cundari E et al. Regulated Ran-binding protein 1 activity is required for organization and function of the mitotic spindle in mammalian cells in vivo. Cell Growth Differ 2000; 11: 455-465.
19. Di Fiore B, Ciciarello M, Mangiacasale R, Palena A, Tassin AM, Cundari E, Lavia P. Mammalian RanBP1 regulates centrosome cohesion during mitosis. J Cell Sci 2003; 116: 3399-3411.
20. Peloponese Jr JM, Haller K, Miyazato A, Jeang KT. Abnormal centrosome amplification in cells through the targeting of Ran-binding protein-1 by the human T cell leukemia virus type-1 Tax oncoprotein. Proc Natl Acad Sci USA 2005; 102: 18974-9.
21. Li HY, Ng WP, Wong CH, Iglesias PA, Zheng Y. Coordination of chromosome alignment and mitotic progression by the chromosome-based Ran signal. Cell Cycle 2007; 6: 1886-1895.
22. Tedeschi A, Ciciarello M, Mangiacasale R, Roscioli E, Rensen WM, Lavia P. RANBP1 localizes a subset of mitotic regulatory factors on spindle microtubules and regulates chromosome segregation in human cells. J Cell Sci 2007; 120: 3748-3761.
23. Ciciarello M, Mangiacasale R, Lavia P. Spatial control of mitosis by the GTPase Ran. Cell Mol Life Sci 2007; 64: 891-914.
24. Kalab P, Heald R. The RanGTP gradient - a GPS for the mitotic spindle. J Cell Sci 2008; 121: 1577-1586.
25. Yuen HF, Chan KK, Grills C, Murray JT, Platt-Higgins AM, Sharaf Eldin O et al. Ran is a potential therapeutic target for cancer cells with molecular changes associated with activation of the PI3K/Akt/mTORC1 and Ras/MEK/ERK pathways. Clin Cancer Res Clin Cancer Res 2012; 18: 380-91.
26. McCaig C, Potter L, Abramczyk O, Murray JT. Phosphorylation of NDRG1 is temporally and spatially controlled during the cell cycle. Biochem Biophys Res Commun 2011; 411: 227-234.
27. Gaspari M, Abbonante V, Cuda G. Gel-free sample preparation for the nanoscale LC-MS/MS analysis and identification of low-nanogram protein samples. Science 2007; 30: 2210-2216.
28. Menniti M, Iuliano R, Amato R, Boito R, Corea M, Le Pera I et al. Serum and glucocorticoid-regulated kinase Sgk1 inhibits insulin-dependent activation of phosphomannomutase 2 in transfected COS-7 cells. Am J Physiol Cell Physiol 2005; 288: C148-55.
29. Menniti M, Iuliano R, Föller M, Sopjani M, Alesutan I, Mariggiò S et al. 60kDa lysophospholipase, a new Sgk1 molecular partner involved in the regulation of ENaC. Cell Physiol Biochem 2010; 26: 587-596.
30. Hardy S, Kitamura M, Harris-Stansil T, Dai Y, Phipps ML. Construction of Adenovirus vectors through Cre-lox recombination. J Virol 1997; 7: 1842-1849.
31. Di Fiore B, Guarguaglini G, Palena A, Kerkhoven RM, Bernards R, Lavia P. Two E2F sites control growth-regulated and cell cycle-regulated transcription of the Htf9-a/RanBP1 gene through functionally distinct mechanisms. J Biol Chem 1999; 274: 10339-10348.
32. Gorman CM, Moffat LF, Howard BH. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol 1982; 2: 1044-1051.
33. Faniello MC, Di Sanzo M, Quaresima B, Baudi F, Di Caro V, Cuda G et al. p53-mediated downregulation of HOURS ferritin promoter transcriptional efficiency via NF-Y. Int J Biochem Cell Biol 2008; 40: 2110-2119.
34. Tan NY, Khachigian LM. Sp1 phosphorylation and its regulation of gene transcription. Mol Cell Biol 2009; 29: 2483-2488.
35. Kim HS, Lim IK. Phosphorylated extracellular signal-regulated protein kinases 1 and 2 phosphorylate sp1 on serine 59 and regulate cellular senescence via transcription of p21Sdi1/Cip1/Waf1. J Biol Chem 2009; 284: 15475-15486.
36. Rensen WM, Roscioli E, Tedeschi A, Mangiacasale R, Ciciarello M, Di Gioia SA et al. RanBP1 downregulation sensitizes cancer cells to taxol in a caspase-3-dependent manner. Oncogene 2009; 28: 1748-1758.
37. Bischoff FR, Krebber HOURS, Smirnova E, Dong W, Ponstingl HOURS. Co-activation of RanGTPase and inhibition of GTP dissociation by Ran-GTP binding protein RanBP1. EMBO J 1995; 14: 705-715.
38. Plafker K, Macara IG. Fluorescence resonance energy transfer biosensors that detect Ran conformational changes and a Ran x GDP-importin-beta -RanBP1 complex in vitro and in intact cells. J Biol Chem 2002; 277: 30121-30127.
39. Clarke PR, Zhang C. Spatial and temporal coordination of mitosis by Ran GTPase. Nat Rev Mol Cell Biol 2008; 9: 464-477.
40. Archer MC. Role of Sp transcription factors in the regulation of cancer. Cell Metabol Genes Cancer 2011; 2: 712-719.
41. Yamada HY, Rao CV. Genes that modulate the sensitivity for anti-microtubule drug-mediated chemotherapy. Curr Cancer Drug Targets 2010; 10: 623-33.
42. Feng Z, Liu L, Zhang C, Zheng T, Wang J, Lin M et al. Chronic restraint stress attenuates p53 function and promotes tumorigenesis. Proc Natl Acad Sci USA 109: 7013-8.