Phosphorylation and changes in the distribution of nucleolin promote tumor metastasis via the PI3K/Akt pathway in colorectal carcinoma

FEBS Letters

Volumn 588, Issue 10, 2014, Pages 1921-1929

  Wu, Dong Ming ^a   Zhang, Peng ^b   Liu, Ru Yan ^c   Sang, Ya Xiong ^a   Zhou, Cong ^a   Xu, Guang Chao ^a   Yang, Jin Liang ^a   Tong, Ai Ping ^a   Wang, Chun Ting ^a  

^a SICHUAN UNIVERSITY   (China)

^b SICHUAN CANCER HOSPITAL   (China)

^c GUANGXI MEDICAL UNIVERSITY   (China)

Author keywords

Colorectal carcinoma; Distribution; Metastatic; Nucleolin; PI3K Akt; VEGF

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; NUCLEOLIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P55; TUMOR MARKER; VASCULOTROPIN;

ADENOCARCINOMA; ADULT; ARTICLE; CANCER STAGING; CELL SURFACE; COLORECTAL CARCINOMA; CONTROLLED STUDY; CORRELATION ANALYSIS; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; METASTASIS; METASTASIS POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

COLORECTAL CARCINOMA; DISTRIBUTION; METASTATIC; NUCLEOLIN; PI3K/AKT; VEGF;

BLOTTING, WESTERN; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; COLORECTAL NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HCT116 CELLS; HUMANS; MALE; MICROSCOPY, FLUORESCENCE; MIDDLE AGED; NEOPLASM METASTASIS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84900448031     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.03.047     Document Type: Article

References (41)

1. S. Bremer, K. Klein, A. Sedlmaier, M. Abouzied, V. Gieselmann, and S. Franken Hepatoma-derived growth factor and nucleolin exist in the same ribonucleoprotein complex BMC Biochem. 14 2013 2
2. S. Cannito, E. Novo, A. Compagnone, L. Valfrè di Bonzo, C. Busletta, and E. Zamara et al. Redox mechanisms switch on hypoxia-dependent epithelial-mesenchymal transition in cancer cells Carcinogenesis 29 2008 2267 2278
3. S. Cascio, R. Ferla, A. D'Andrea, A. Gerbino, V. Bazan, and E. Surmacz et al. Expression of angiogenic regulators, VEGF and leptin, is regulated by the EGF/PI3K/STAT3 pathway in colorectal cancer cells J. Cell. Physiol. 221 2009 189 194
4. V.P. Chekhonin, S.A. Shein, and A.A. Korchagina GurinaOI. VEGF in tumor progression and targeted therapy Curr. Cancer Drug Targets 13 2013 423 443
5. S. Christian, J. Pilch, M.E. Akerman, K. Porkka, P. Laakkonen, and E. Ruoslahti Nucleolin expressed at the cell surface is a marker of endothelial cells in angiogenic blood vessels J. Cell Biol. 4 2003 871 878
6. Y. Ding, N. Song, C. Liu, T. He, W. Zhuo, and X. He et al. Heat shock cognate 70 regulates the translocation and angiogenic function of nucleolin Arterioscler. Thromb. Vasc. Biol. 32 2012 e126 e134
7. D. El Khoury, D. Destouches, R. Lengagne, B. Krust, Y. Hamma-Kourbali, and M. Garcette et al. Targeting surface nucleolin with a multivalent pseudopeptide delays development of spontaneous melanoma in RET transgenic mice BMC Cancer 10 2010 325 337
8. K. Farin, S. Schokoroy, R. Haklai, I. Cohen-Or, G. Elad-Sfadia, and M.E. Reyes-Reyes et al. Oncogenic synergism between ErbB1, nucleolin, and mutant Ras Cancer Res. 6 2011 2040 2051
9. J. Ferlay, I. Soerjomataram, M. Ervik, R. Dikshit, S. Eser, C. Mathers, et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet].
10. G. Gliki, C. Wheeler-Jones, and I. Zachary Vascular endothelial growth factor induces protein kinase C (PKC)-dependent Akt/PKB activation and phosphatidylinositol 3′-kinase-mediates PKC delta phosphorylation: role of PKC in angiogenesis Cell Biol. Int. 26 2002 751 759
11. A. Hovanessian, C. Soundaramourty, D. El Khoury, I. Nondier, J. Svab, and B. Krust Surface expressed nucleolin is constantly induced in tumor cells to mediate calcium-dependent ligand internalization PLoS ONE 5 12 2010 e15787
12. J. Hu, X. Xia, A. Cheng, G. Wang, X. Luo, and M.F. Reed et al. A peptide inhibitor derived from p55PIK phosphatidylinositol 3-kinase regulatory subunit: a novel cancer therapy Mol. Cancer Ther. 7 2008 3719 3728
13. Y. Huang, H. Shi, H. Zhou, X. Song, S. Yuan, and Y. Luo The angiogenic function of nucleolin is mediated by vascular endothelial growth factor and nonmuscle myosin Blood 107 2006 3564 3571
14. C.J. Huang, H.W. Teng, C.C. Chien, J.K. Lin, and S.H. Yang Prognostic significance of C - reactive protein polymorphism and KRAS/BRAF in synchronous liver metastasis from colorectal cancer PLoS ONE 8 2013 e65117
15. J.P. Huddleson, N. Ahmad, and J.B. Lingrel Up-regulation of the KLF2 transcription factor by fluid shear stress requires nucleolin J. Biol. Chem. 281 2006 15121 15128
16. H. Kiefel, S. Bondong, M. Pfeifer, U. Schirmer, N. Erbe-Hoffmann, and H. Schäfer et al. EMT-associated up-regulation of L1CAM provides insights into L1CAM-mediated integrin signaling and NF-kappaB activation Carcinogenesis 33 2012 1919 1929
17. M. Koutsioumpa, C. Polytarchou, J. Courty, Y. Zhang, N. Kieffer, and C. Mikelis et al. Interplay between alphavbeta3 integrin and nucleolin regulates human endothelial and glioma cell migration J. Biol. Chem. 288 2013 343 354
18. Y. Lee, A. Marquez, O. Mungunsukh, and R. Day Hepatocyte growth factor inhibits apoptosis by the profibrotic factor angiotensin II via extracellular signal-regulated kinase 1/2 in endothelial cells and tissue explants Mol. Biol. Cell 23 2010 4240 4250
19. Lyon, France. International Agency for Research on Cancer 2013. Available from: < http://globocan.iarc.fr > (accessed day/month/year.).
20. E.H. Nam, Y. Lee, Y.K. Park, J.W. Lee, and S. Kim ZEB2 upregulates integrin alpha5 expression through cooperation with Sp1 to induce invasion during epithelial-mesenchymal transition of human cancer cells Carcinogenesis 33 2012 563 571
21. L. Peng, J. Liang, H. Wang, X. Song, A. Rashid, and H.F. Gomez et al. High levels of nucleolar expression of nucleolin are associated with better prognosis in patients with stage II pancreatic ductal adenocarcinoma Clin. Cancer Res. 16 2010 3734 3742
22. F. Pichiorri, D. Palmieri, L. De Luca, J. Consiglio, J. You, and A. Rocci et al. In vivo NCL targeting affects breast cancer aggressiveness through miRNA regulation J. Exp. Med. 210 2013 951 968
23. W. Qiu, F. Zhou, Q. Zhang, X. Sun, X. Shi, and Y. Liang et al. Overexpression of nucleolin and different expression sites both related to the prognosis of gastric cancer APMIS 2013 10.1111/apm.12131
24. E.M. Reyes-Reyes, and S.K. Akiyama Cell-surface nucleolin is a signal transducing P-selectin binding protein for human colon carcinoma cells Exp. Cell Res. 314 2008 2212 2223
25. Rebecca Siegel, Deepa Naishadham, and Ahmedin Jemal Cancer Statistics CA Cancer J. Clin. 2013 63 2013 11 30
26. S. Saigusa, Y. Inoue, K. Tanaka, Y. Toiyama, Y. Okugawa, and T. Shimura et al. Decreased expression of DUSP4 is associated with liver and lung metastases in colorectal cancer Med. Oncol. 30 2013 620
27. S. Semba, E. Mizuuchi, and H. Yokozaki Requirement of phosphatase of regenerating liver-3 for the nucleolar localization of nucleolin during the progression of colorectal carcinoma Cancer Sci. 10 2010 2254 2261
28. N. Song, Y. Ding, W. Zhuo, T. He, Z. Fu, and Y. Chen et al. The nuclear translocation of endostatin is mediated by its receptor nucleolin in endothelial cells Angiogenesis 4 2012 697 711
29. S. Storck, M. Shukla, S. Dimitrov, and P. Bouvet Functions of the histone chaperone nucleolin in diseases Subcell. Biochem. 41 2007 125 144
30. N. Turck, O. Lefebvre, I. Gross, P. Gendry, M. Kedinger, and P. Simon-Assmann Effect of laminin-1 on intestinal cell differentiation involves inhibition of nuclear nucleolin J. Cell. Physiol. 2 2006 545 555
31. J.F. Wise, Z. Berkova, R. Mathur, H. Zhu, F.K. Braun, and R.H. Tao et al. Nucleolin inhibits Fas ligand binding and suppresses Fas-mediated apoptosis in vivo via a surface nucleolin-Fas complex Blood 121 2013 4729 4739
32. C.D. Wu, H.W. Chou, Y.S. Kuo, R.M. Lu, Y.C. Hwang, and H.C. Wu et al. Nucleolin antisense oligodeoxynucleotides induce apoptosis and may be used as a potential drug for nasopharyngeal carcinoma therapy Oncol. Rep. 27 2012 94 100
33. K. Abdelmohsen, and M. Gorospe RNA-binding protein nucleolin in disease RNA Biol. 9 6 2012 799 808
34. J.W. Zinser-Sierra, S. Rodríguez-Ramírez, R. Villalobos-Valencia, and M. Ramírez-Márquez Use of bevacizumab in metastatic colorectal cancer: report from the Mexican opinion and analysis forum on colorectal cancer treatment with bevacizumab (September 2009) Drugs R D 11 2011 101 111
35. I. Dumler, V. Stepanova, U. Jerke, O.A. Mayboroda, F. Vogel, and P. Bouvet et al. Urokinase-induced mitogenesis is mediated by casein kinase 2 and nucleolin Curr. Biol. 9 1999 1468 1476
36. M. Fahling, A. Steege, A. Perlewitz, B. Nafz, R. Mrowka, and P.B. Persson et al. Role of nucleolin in posttranscriptional control of MMP-9 expression Biochim. Biophys. Acta 1731 2005 32 40
37. P.S. Hegde, A.M. Jubb, D. Chen, N.F. Li, Y.G. Meng, and C. Bernaards et al. Predictive impact of circulating vascular endothelial growth factor in four phase III trials evaluating bevacizumab Clin. Cancer Res. 19 2013 929 937
38. L.M. Litchfield, K.A. Riggs, A.M. Hockenberry, L.D. Oliver, K.G. Barnhart, and J. Cai et al. Identification and characterization of nucleolin as a COUP-TFII coactivator of retinoic acid receptor beta transcription in breast cancer cells PLoS ONE 7 2012 e38278
39. E.M. Reyes-Reyes, Y. Teng, and P.J. Bates A new paradigm for aptamer therapeutic AS1411 action: uptake by macropinocytosis and its stimulation by a nucleolin-dependent mechanism Cancer Res. 70 2010 8617 8629
40. A.J. Weickhardt, N.C. Tebbutt, and J.M. Mariadason Strategies for overcoming inherent and acquired resistance to EGFR inhibitors by targeting downstream effectors in the RAS/PI3K pathway Curr. Cancer Drug Targets 10 2010 824 833
41. Q. Xu, Q. Sun, J. Zhang, J. Yu, W. Chen, and Z. Zhang Downregulation of miR-153 contributes to epithelial-mesenchymal transition and tumor metastasis in human epithelial cancer Carcinogenesis 34 2013 539 549