Table of Contents Author Guidelines Submit a Manuscript
International Journal of Cell Biology
Volume 2009, Article ID 243532, 11 pages
http://dx.doi.org/10.1155/2009/243532
Research Article

The N-Terminal Domain of Y-Box Binding Protein-1 Induces Cell Cycle Arrest in G2/M Phase by Binding to Cyclin D1

Department of Molecular Sciences, The University of Tennessee Health Science Center, Memphis, TN 38163, USA

Received 1 November 2009; Accepted 31 December 2009

Academic Editor: David Bazett-Jones

Copyright © 2009 Payal Khandelwal et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. Kohno, H. Izumi, T. Uchiumi, M. Ashizuka, and M. Kuwano, “The pleiotropic functions of the Y-box-binding protein, YB-1,” BioEssays, vol. 25, no. 7, pp. 691–698, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Ladomery, “Multifunctional proteins suggest connections between transcriptional and post-transcriptional processes,” BioEssays, vol. 19, no. 10, pp. 903–909, 1997. View at Google Scholar · View at Scopus
  3. K. Matsumoto and A. P. Wolffe, “Gene regulation by Y-box proteins: coupling control of transcription and translation,” Trends in Cell Biology, vol. 8, no. 8, pp. 318–323, 1998. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Sommerville, “Activities of cold-shock domain proteins in translation control,” BioEssays, vol. 21, no. 4, pp. 319–325, 1999. View at Google Scholar · View at Scopus
  5. S. Das, R. Chattopadhyay, K. K. Bhakat et al., “Stimulation of NEIL2-mediated oxidized base excision repair via YB-1 interaction during oxidative stress,” Journal of Biological Chemistry, vol. 282, no. 39, pp. 28474–28484, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. R. C. Bargou, K. Jürchott, C. Wagener et al., “Nuclear localization and increased levels of transcription factor YB-1 in primary human breast cancers are associated with intrinsic MDR1 gene expression,” Nature Medicine, vol. 3, no. 4, pp. 447–450, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Janz, N. Harbeck, P. Dettmar et al., “Y-box factor YB-1 predicts drug resistance and patient outcome in breast cancer independent of clinically relevant tumor biologic factors HER2, uPA and PAI-1,” International Journal of Cancer, vol. 97, no. 3, pp. 278–282, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. U. Stein, K. Jürchott, W. Walther, S. Bergmann, P. M. Schlag, and H.-D. Royer, “Hyperthermia-induced nuclear translocation of transcription factor YB-1 leads to enhanced expression of multidrug resistance-related ABC transporters,” Journal of Biological Chemistry, vol. 276, no. 30, pp. 28562–28569, 2001. View at Publisher · View at Google Scholar · View at Scopus
  9. J.-L. Duh, H. Zhu, H. G. Shertzer, D. W. Nebert, and A. Puga, “The Y-box motif mediates redox-dependent transcriptional activation in mouse cells,” Journal of Biological Chemistry, vol. 270, no. 51, pp. 30499–30507, 1995. View at Publisher · View at Google Scholar · View at Scopus
  10. S. K. Swamynathan, A. Nambiar, and R. V. Guntaka, “Role of single-stranded DNA regions and Y-box proteins in transcriptional regulation of viral and cellular genes,” FASEB Journal, vol. 12, no. 7, pp. 515–522, 1998. View at Google Scholar · View at Scopus
  11. Z. H. Lu, J. T. Books, and T. J. Ley, “YB-1 is important for late-stage embryonic development, optimal cellular stress responses, and the prevention of premature senescence,” Molecular and Cellular Biology, vol. 25, no. 11, pp. 4625–4637, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. T. Uchiumi, A. Fotovati, T. Sasaguri et al., “YB-1 is important for an early stage embryonic development: neural tube formation and cell proliferation,” Journal of Biological Chemistry, vol. 281, no. 52, pp. 40440–40449, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Ladomery and J. Sommerville, “A role for Y-box proteins in cell proliferation,” BioEssays, vol. 17, no. 1, pp. 9–11, 1995. View at Google Scholar · View at Scopus
  14. A. En-Nia, E. Yilmaz, U. Klinge, D. H. Lovett, I. Stefanidis, and P. R. Mertens, “Transcription factor YB-1 mediates DNA polymerase α gene expression,” Journal of Biological Chemistry, vol. 280, no. 9, pp. 7702–7711, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Gu, T. Oyama, T. Osaki, K. Kohno, and K. Yasumoto, “Expression of Y box-binding protein-1 correlates with DNA topoisomerase IIα and proliferating cell nuclear antigen expression in lung cancer,” Anticancer Research, vol. 21, no. 4, pp. 2357–2362, 2001. View at Google Scholar · View at Scopus
  16. T. Ise, G. Nagatani, T. Imamura et al., “Transcription factor Y-box binding protein 1 binds preferentially to cisplatin-modified DNA and interacts with proliferating cell nuclear antigen,” Cancer Research, vol. 59, no. 2, pp. 342–346, 1999. View at Google Scholar · View at Scopus
  17. K. Shibao, H. Takano, Y. Nakayama et al., “Enhanced coexpression of YB-1 and DNA topoisomerase II a genes in human colorectal carcinomas,” International Journal of Cancer, vol. 83, no. 6, pp. 732–737, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. S. K. Swamynathan, B. R. Varma, K. T. Weber, and R. V. Guntaka, “Targeted disruption of one allele of the Y-box protein gene, Chk-YB-1b, in DT40 cells results in major defects in cell cycle,” Biochemical and Biophysical Research Communications, vol. 296, no. 2, pp. 451–457, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Matsumoto, K. J. Tanaka, and M. Tsujimoto, “An acidic protein, YBAP1, mediates the release of YB-1 from mRNA and relieves the translational repression activity of YB-1,” Molecular and Cellular Biology, vol. 25, no. 5, pp. 1779–1792, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Shibahara, T. Uchiumi, T. Fukuda et al., “Targeted disruption of one allele of the Y-box binding protein-1 (YB-1) gene in mouse embryonic stem cells and increased sensitivity to cisplatin and mitomycin C,” Cancer Science, vol. 95, no. 4, pp. 348–353, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. B. Schittek, K. Psenner, B. Sauer, F. Meier, T. Iftner, and C. Garbe, “The increased expression of Y box-binding protein 1 in melanoma stimulates proliferation and tumor invasion, antagonizes apoptosis and enhances chemoresistance,” International Journal of Cancer, vol. 120, no. 10, pp. 2110–2118, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Sambrook and D. W. Russell, Molecular Cloning: A Labarotory Manual, vol. 3, chapter 15.51, Cold Spring Harbor, Cold Spring Harbor, NY, USA, 2001.
  23. P. A. Crawford, N. Sharma, S. Chandrasekar et al., “Over-expression, purification, and characterization of metallo-ß-lactamase ImiS from Aeromonas veronii bv. sobria,” Protein Expression and Purification, vol. 36, no. 2, pp. 272–279, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. V. A. J. Smits, R. Klompmaker, T. Vallenius, G. Rijksen, T. P. Makela, and R. H. Medema, “p21 inhibits Thr161 phosphorylation of Cdc2 to enforce the G2 DNA damage checkpoint,” Journal of Biological Chemistry, vol. 275, no. 39, pp. 30638–30643, 2000. View at Google Scholar · View at Scopus
  25. D. Derossi, S. Calvet, A. Trembleau, A. Brunissen, G. Chassaing, and A. Prochiantz, “Cell internalization of the third helix of the antennapedia homeodomain is receptor-independent,” Journal of Biological Chemistry, vol. 271, no. 30, pp. 18188–18193, 1996. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Chiesa, E. Rapizzi, V. Tosello et al., “Recombinant aequorin and green fluorescent protein as valuable tools in the study of cell signalling,” Biochemical Journal, vol. 355, no. 1, pp. 1–12, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Jürchott, S. Bergmann, U. Stein et al., “YB-1 as a cell cycle-regulated transcription factor facilitating cyclin A and cyclin B1 gene expression,” Journal of Biological Chemistry, vol. 278, no. 30, pp. 27988–27996, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. C. E. Grant and R. G. Deeley, “Cloning and characterization of chicken YB-1: regulation of expression in the liver,” Molecular and Cellular Biology, vol. 13, no. 7, pp. 4186–4196, 1993. View at Google Scholar · View at Scopus
  29. J. C. Kandala and R. V. Guntaka, “Cloning of Rous sarcoma virus enhancer factor genes. I. Evidence that RSV- EF-1 is related to Y-box (inverted CCAAT) binding proteins and binds to multiple motifs in the RSV enhancer,” Virology, vol. 198, no. 1, pp. 514–523, 1994. View at Google Scholar · View at Scopus
  30. S. W. Jones, R. Christison, K. Bundell et al., “Characterisation of cell-penetrating peptide-mediated peptide delivery,” British Journal of Pharmacology, vol. 145, no. 8, pp. 1093–1102, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Fu, C. Wang, Z. Li, T. Sakamaki, and R. G. Pestell, “Cyclin D1: normal and abnormal functions,” Endocrinology, vol. 145, no. 12, pp. 5439–5447, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. J. K. Kim and J. A. Diehl, “Nuclear cyclin D1: an oncogenic driver in human cancer,” Journal of Cellular Physiology, vol. 220, no. 2, pp. 292–296, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. D. W. Stacey, “Cyclin D1 serves as a cell cycle regulatory switch in actively proliferating cells,” Current Opinion in Cell Biology, vol. 15, no. 2, pp. 158–163, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. D. W. Stacey and M. Hitomi, “Cell cycle studies based upon quantitative image analysis,” Cytometry A, vol. 73, no. 4, pp. 270–278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Kozar, M. A. Ciemerych, V. I. Rebel et al., “Mouse development and cell proliferation in the absence of D-cyclins,” Cell, vol. 118, no. 4, pp. 477–491, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. B. Chen and J. W. Pollard, “Cyclin D2 compensates for the loss of cyclin D1 in estrogen-induced mouse uterine epithelial cell proliferation,” Molecular Endocrinology, vol. 17, no. 7, pp. 1368–1381, 2003. View at Publisher · View at Google Scholar · View at Scopus
  37. C. J. Sherr, “D1 in G2,” Cell Cycle, vol. 1, no. 1, pp. 36–38, 2002. View at Google Scholar · View at Scopus
  38. K. Yang, M. Hitomi, and D. W. Stacey, “Variations in cyclin D1 levels through the cell cycle determine the proliferative fate of a cell,” BMC Cell Division, vol. 1, pp. 32–39, 2006. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Astanehe, M. R. Finkbeiner, P. Hojabrpour et al., “The transcriptional induction of PIK3CA in tumor cells is dependent on the oncoprotein Y-box binding protein-1,” Oncogene, vol. 28, no. 25, pp. 2406–2418, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. A. G. Bader and P. K. Vogt, “Phosphorylation by Akt disables the anti-oncogenic activity of YB-1,” Oncogene, vol. 27, no. 8, pp. 1179–1182, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. B. W. Sutherland, J. Kucab, J. Wu et al., “Akt phosphorylates the Y-box binding protein 1 at Ser102 located in the cold shock domain and affects the anchorage-independent growth of breast cancer cells,” Oncogene, vol. 24, no. 26, pp. 4281–4292, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. V. Evdokimova, L. P. Ovchinnikov, and P. H. B. Sorensen, “Y-box binding protein 1: providing a new angle on translational regulation,” Cell Cycle, vol. 5, no. 11, pp. 1143–1147, 2006. View at Google Scholar · View at Scopus
  43. F. Takahashi-Yanaga and T. Sasaguri, “GSK-3β regulates cyclin D1 expression: a new target for chemotherapy,” Cellular Signalling, vol. 20, no. 4, pp. 581–589, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. M. R. Finkbeiner, A. Astanehe, K. To et al., “Profiling YB-1 target genes uncovers a new mechanism for MET receptor regulation in normal and malignant human mammary cells,” Oncogene, vol. 28, no. 11, pp. 1421–1431, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. T. Okamoto, H. Izumi, T. Imamura et al., “Direct interaction of p53 with the Y-box binding protein, YB-1: a mechanism for regulation of human gene expression,” Oncogene, vol. 19, no. 54, pp. 6194–6202, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Lobrich and P. A. Jeggo, “The impact of a negligent G2/M checkpoint on genomic instability and cancer induction,” Nature Reviews Cancer, vol. 7, no. 11, pp. 861–869, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. P. V. Ruzanov, V. M. Evdokimova, N. L. Korneeva, J. W. B. Hershey, and L. P. Ovchinnikov, “Interaction of the universal mRNA-binding protein, p50, with actin: a possible link between mRNA and microfilaments,” Journal of Cell Science, vol. 112, no. 20, pp. 3487–3496, 1999. View at Google Scholar · View at Scopus
  48. M. Piel, J. Nordberg, U. Euteneur, and M. Bornens, “Centrosome-dependent exit of cytokinesis in animal cells,” Science, vol. 291, no. 5508, pp. 1550–1553, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. E. A. Nigg, “Centrosome aberrations: cause or consequence of cancer progression?” Nature Reviews Cancer, vol. 2, no. 11, pp. 815–825, 2002. View at Publisher · View at Google Scholar · View at Scopus