Calcineurin-mediated YB-1 dephosphorylation regulates CCL5 expression during monocyte differentiation

Journal of Biological Chemistry

Volumn 289, Issue 31, 2014, Pages 21401-21412

  Alidousty, Christina ^a   Rauen, Thomas ^a   Hanssen, Lydia ^a   Wang, Qiang ^b   Alampour Rajabi, Setareh ^a   Mertens, Peter R ^c   Bernhagen, Jürgen ^a   Floege, Jürgen ^a   Ostendorf, Tammo ^a   Raffetseder, Ute ^a  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b NANJING MEDICAL UNIVERSITY   (China)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BINDING ENERGY; BODY FLUIDS; CHEMICAL ACTIVATION; GENES; PROTEINS; TRANSCRIPTION;

DIFFERENTIATION PROCESS; GENE TRANSCRIPTIONS; IMMUNOPRECIPITATION ASSAYS; INFLAMMATORY PROCESS; MACROPHAGE DIFFERENTIATIONS; PHORBOL MYRISTATE ACETATES; POST-TRANSLATIONAL MODIFICATIONS; TRANSCRIPTIONAL TARGETS;

PHOSPHORYLATION;

CALCINEURIN; CYCLOSPORIN; INTERCELLULAR ADHESION MOLECULE 1; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE B; RANTES; SERINE; Y BOX BINDING PROTEIN 1; CCL5 PROTEIN, HUMAN; PRIMER DNA; YBX1 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; FEMALE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INFLAMMATION; KIDNEY DISEASE; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RAT; SIGNAL TRANSDUCTION; TRANSACTIVATION; WESTERN BLOTTING; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; PHYSIOLOGY; POLYMERASE CHAIN REACTION;

BASE SEQUENCE; CALCINEURIN; CELL DIFFERENTIATION; CELL LINE; CHEMOKINE CCL5; DNA PRIMERS; HUMANS; MONOCYTES; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; TETRADECANOYLPHORBOL ACETATE; Y-BOX-BINDING PROTEIN 1;

EID: 84905384542     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.562991     Document Type: Article

References (39)

1. Nardozzi, J. D., Lott, K., and Cingolani, G. (2010) Phosphorylation meets nuclear import: a review. Cell Commun. Signal 8, 32
2. Seo, J., and Lee, K. J. (2004) Post-translational modifications and their biological functions: proteomic analysis and systematic approaches. J. Biochem. Mol. Biol. 37, 35-44 (Pubitemid 38402572)
3. Jain, J., McCaffrey, P. G., Miner, Z., Kerppola, T. K., Lambert, J. N., Verdine, G. L., Curran, T., and Rao, A. (1993) The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature 365, 352-355 (Pubitemid 23288978)
4. Rao, A., Luo, C., and Hogan, P. G. (1997) Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15, 707-747 (Pubitemid 27169297)
5. Burke, B. A., Chavers, B. M., Gillingham, K. J., Kashtan, C. E., Manivel, J. C., Mauer, S. M., Nevins, T. E., and Matas, A. J. (1995) Chronic renal allograft rejection in the first 6 months posttransplant. Transplantation 60, 1413-1417 (Pubitemid 26012672)
6. Hariharan, S., Johnson, C. P., Bresnahan, B. A., Taranto, S. E., McIntosh, M. J., and Stablein, D. (2000) Improved graft survival after renal transplantation in the United States, 1988 to 1996. N. Engl. J. Med. 342, 605-612 (Pubitemid 30118412)
7. Mihatsch, M. J., Kyo, M., Morozumi, K., Yamaguchi, Y., Nickeleit, V., and Ryffel, B. (1998) The side-effects of ciclosporine-A and tacrolimus. Clin. Nephrol. 49, 356-363 (Pubitemid 28271466)
8. Hanssen, L., Frye, B. C., Ostendorf, T., Alidousty, C., Djudjaj, S., Boor, P., Rauen, T., Floege, J., Mertens, P. R., and Raffetseder, U. (2011) Y-Box Binding Protein-1 Mediates Profibrotic Effects of Calcineurin Inhibitors in the Kidney. J. Immunol. 187, 298-308
9. Mertens, P. R., Alfonso-Jaume, M. A., Steinmann, K., and Lovett, D. H. (1999) YB-1 regulation of the human and rat gelatinase A genes via similar enhancer elements. J. Am. Soc. Nephrol. 10, 2480-2487
10. En-Nia, A., Yilmaz, E., Klinge, U., Lovett, D. H., Stefanidis, I., and Mertens, P. R. (2005) Transcription factor YB-1 mediates DNA polymerase α gene expression. J. Biol. Chem. 280, 7702-7711 (Pubitemid 40349663)
11. Raffetseder, U., Frye, B., Rauen, T., Jürchott, K., Royer, H. D., Jansen, P. L., and Mertens, P. R. (2003) Splicing factor SRp30c interaction with Y-box protein-1 confers nuclear YB-1 shuttling and alternative splice site selection. J. Biol. Chem. 278, 18241-18248 (Pubitemid 36799442)
12. Chen, C. Y., Gherzi, R., Andersen, J. S., Gaietta, G., Jürchott, K., Royer, H. D., Mann, M., and Karin, M. (2000) Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev. 14, 1236-1248 (Pubitemid 30327504)
13. Sinnberg, T., Sauer, B., Holm, P., Spangler, B., Kuphal, S., Bosserhoff, A., and Schittek, B. (2012) MAPK and PI3K/AKT mediated YB-1 activation promotes melanoma cell proliferation which is counteracted by an auto-regulatory loop. Exp. Dermatol. 21, 265-270
14. Wu, J., Stratford, A. L., Astanehe, A., and Dunn, S. E. (2007) YB-1 is a Transcription/Translation Factor that Orchestrates the Oncogenome by Hardwiring Signal Transduction to Gene Expression. Transl. Oncogenomics 2, 49-65
15. Allemand, E., Hastings, M. L., Murray, M. V., Myers, M. P., and Krainer, A. R. (2007) Alternative splicing regulation by interaction of phosphatase PP2Cγ with nucleic acid-binding protein YB-1. Nat. Struct. Mol. Biol. 14, 630-638 (Pubitemid 47037064)
16. Hanssen, L., Alidousty, C., Djudjaj, S., Frye, B. C., Rauen, T., Boor, P., Mertens, P. R., van Roeyen, C. R., Tacke, F., Heymann, F., Tittel, A. P., Koch, A., Floege, J., Ostendorf, T., and Raffetseder, U. (2013) YB-1 Is an Early and Central Mediator of Bacterial and Sterile Inflammation In Vivo. J. Immunol. 191, 2604-2613
17. Raffetseder, U., Rauen, T., Djudjaj, S., Kretzler, M., En-Nia, A., Tacke, F., Zimmermann, H. W., Nelson, P. J., Frye, B. C., Floege, J., Stefanidis, I., Weber, C., and Mertens, P. R. (2009) Differential regulation of chemokine CCL5 expression in monocytes/macrophages and renal cells by Y-box protein-1. Kidney Int. 75, 185-196
18. Krohn, R., Raffetseder, U., Bot, I., Zernecke, A., Shagdarsuren, E., Liehn, E. A., van Santbrink, P. J., Nelson, P. J., Biessen, E. A., Mertens, P. R., and Weber, C. (2007) Y-box binding protein-1 controls CC chemokine ligand-5 (CCL5) expression in smooth muscle cells and contributes to neointima formation in atherosclerosis-prone mice. Circulation 116, 1812-1820 (Pubitemid 350287106)
19. Wilson, H. M., Walbaum, D., and Rees, A. J. (2004) Macrophages and the kidney. Curr Opin. Nephrol. Hypertens 13, 285-290 (Pubitemid 38582301)
20. Shi, C., and Simon, D. I. (2006) Integrin signals, transcription factors, and monocyte differentiation. Trends Cardiovasc. Med. 16, 146-152 (Pubitemid 43867327)
21. Raffetseder, U., Liehn, E. A., Weber, C., and Mertens, P. R. (2012) Role of cold shock Y-box protein-1 in inflammation, atherosclerosis and organ transplant rejection. Eur. J. Cell Biol. 91, 567-575
22. Shibasaki, F., Price, E. R., Milan, D., and McKeon, F. (1996) Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature 382, 370-373 (Pubitemid 26260467)
23. Hallhuber, M., Burkard, N., Wu, R., Buch, M. H., Engelhardt, S., Hein, L., Neyses, L., Schuh, K., and Ritter, O. (2006) Inhibition of nuclear import of calcineurin prevents myocardial hypertrophy. Circ. Res. 99, 626-635 (Pubitemid 44401454)
24. MacDonald, G. H., Itoh-Lindstrom, Y., and Ting, J. P. (1995) The transcriptional regulatory protein, YB-1, promotes single-stranded regions in the DRA promoter. J. Biol. Chem. 270, 3527-3533
25. Rauen, T., Raffetseder, U., Frye, B. C., Djudjaj, S., Mühlenberg, P. J., Eitner, F., Lendahl, U., Bernhagen, J., Dooley, S., and Mertens, P. R. (2009) YB-1 acts as a ligand for Notch-3 receptors and modulates receptor activation. J. Biol. Chem. 284, 26928-26940
26. Tsuchiya, S., Kobayashi, Y., Goto, Y., Okumura, H., Nakae, S., Konno, T., and Tada, K. (1982) Induction of maturation in cultured human monocytic leukemia cells by a phorbol diester. Cancer Res. 42, 1530-1536 (Pubitemid 12148801)
27. Stratford, A. L., Fry, C. J., Desilets, C., Davies, A. H., Cho, Y. Y., Li, Y., Dong, Z., Berquin, I. M., Roux, P. P., and Dunn, S. E. (2008) Y-box binding pro-tein- 1 serine 102 is a downstream target of p90 ribosomal S6 kinase in basal-like breast cancer cells. Breast Cancer Res. 10, R99
28. Sutherland, B. W., Kucab, J., Wu, J., Lee, C., Cheang, M. C., Yorida, E., Turbin, D., Dedhar, S., Nelson, C., Pollak, M., Leighton Grimes, H., Miller, K., Badve, S., Huntsman, D., Blake-Gilks, C., Chen, M., Pallen, C. J., and Dunn, S. E. (2005) 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 24, 4281-4292 (Pubitemid 40961781)
29. Evdokimova, V., Ruzanov, P., Anglesio, M. S., Sorokin, A. V., Ovchinnikov, L. P., Buckley, J., Triche, T. J., Sonenberg, N., and Sorensen, P. H. (2006) Akt-mediated YB-1 phosphorylation activates translation of silent mRNA species. Mol. Cell. Biol. 26, 277-292
30. Basaki, Y., Hosoi, F., Oda, Y., Fotovati, A., Maruyama, Y., Oie, S., Ono, M., Izumi, H., Kohno, K., Sakai, K., Shimoyama, T., Nishio, K., and Kuwano, M. (2007) Akt-dependent nuclear localization of Y-box-binding protein 1 in acquisition of malignant characteristics by human ovarian cancer cells. Oncogene 26, 2736-2746 (Pubitemid 46663838)
31. Capowski, E. E., Esnault, S., Bhattacharya, S., and Malter, J. S. (2001) Y box-binding factor promotes eosinophil survival by stabilizing granulocyte-macrophage colony-stimulating factor mRNA. J. Immunol. 167, 5970-5976 (Pubitemid 33062794)
32. Mertens, P. R., Alfonso-Jaume, M. A., Steinmann, K., and Lovett, D. H. (1998) A synergistic interaction of transcription factors AP2 and YB-1 regulates gelatinase A enhancer-dependent transcription. J. Biol. Chem. 273, 32957-32965 (Pubitemid 28557689)
33. Diamond, P., Shannon, M. F., Vadas, M. A., and Coles, L. S. (2001) Cold shock domain factors activate the granulocyte-macrophage colony-stimulating factor promoter in stimulated Jurkat T cells. J. Biol. Chem. 276, 7943-7951
34. Baksh, S., DeCaprio, J. A., and Burakoff, S. J. (2000) Calcineurin regulation of the mammalian G0/G1 checkpoint element, cyclin-dependent kinase 4. Oncogene 19, 2820-2827 (Pubitemid 30386418)
35. Garcia-Cozar, F. J., Okamura, H., Aramburu, J. F., Shaw, K. T., Pelletier, L., Showalter, R., Villafranca, E., and Rao, A. (1998) Two-site interaction of nuclear factor of activated T cells with activated calcineurin. J. Biol. Chem. 273, 23877-23883 (Pubitemid 28435724)
36. Wang, J., Liu, S., Haditsch, U., Tu, W., Cochrane, K., Ahmadian, G., Tran, L., Paw, J., Wang, Y., Mansuy, I., Salter, M. M., and Lu, Y. M. (2003) Interaction of calcineurin and type-A GABA receptor γ 2 subunits produces long-term depression at CA1 inhibitory synapses. J Neurosci. 23, 826-836 (Pubitemid 36206173)
37. Stratford, A. L., Habibi, G., Astanehe, A., Jiang, H., Hu, K., Park, E., Shadeo, A., Buys, T. P., Lam, W., Pugh, T., Marra, M., Nielsen, T. O., Klinge, U., Mertens, P. R., Aparicio, S., and Dunn, S. E. (2007) Epidermal growth factor receptor (EGFR) is transcriptionally induced by the Y-box binding protein-1 (YB-1) and can be inhibited with Iressa in basal-like breast cancer, providing a potential target for therapy. Breast Cancer Res. 9, R61
38. Boehlk, S., Fessele, S., Mojaat, A., Miyamoto, N. G., Werner, T., Nelson, E. L., Schlöndorff, D., and Nelson, P. J. (2000) ATF and Jun transcription factors, acting through an Ets/CRE promoter module, mediate lipopolysaccharide inducibility of the chemokine RANTES in monocytic Mono Mac 6 cells. Eur. J. Immunol. 30, 1102-1112 (Pubitemid 30216227)
39. 2+ channel activity and nuclear signaling. Neuron 55, 261-275