Cold shock Y-box protein-1 proteolysis autoregulates its transcriptional activities

Cell Communication and Signaling

Volumn 11, Issue 1, 2013, Pages

  Van Roeyen, Claudia R C ^a   Scurt, Florian G ^b   Brandt, Sabine ^b   Kuhl, Vanessa A ^a   Martinkus, Sandra ^a   Djudjaj, Sonja ^b   Raffetseder, Ute ^a   Royer, Hans Dieter ^c   Stefanidis, Ioannis ^d   Dunn, Sandra E ^e   Dooley, Steven ^f   Weng, Honglei ^f   Fischer, Thomas ^b   Lindquist, Jonathan A ^b   Mertens, Peter R ^b  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c CENTER OF ADVANCED EUROPEAN STUDIES AND RESEARCH CAESAR   (Germany)

^d UNIVERSITY OF THESSALY   (Greece)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^f UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Cold shock protein; DbpB; Nuclear localization signal; Post translational modification; RNA DNA binding protein; YBX1

Indexed keywords

COLD SHOCK PROTEIN; COLD SHOCK Y BOX PROTEIN 1; COLLAGEN TYPE 1; DNA BINDING PROTEIN; GELATINASE A; PROTEASOME; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; Y BOX BINDING PROTEIN 1;

ANIMAL CELL; ARTICLE; AUTOREGULATION; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELL NUCLEUS; CELLULAR DISTRIBUTION; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; RAT; TRANSCRIPTION INITIATION; ANIMAL; CELL CULTURE; CELL LINE; CHEMISTRY; GENETIC TRANSCRIPTION; HUMAN; MESANGIUM CELL; METABOLISM; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; HUMANS; MESANGIAL CELLS; NUCLEAR EXPORT SIGNALS; NUCLEAR LOCALIZATION SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTEOLYSIS; RATS; TRANSCRIPTION, GENETIC; Y-BOX-BINDING PROTEIN 1;

EID: 84883580090     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/1478-811X-11-63     Document Type: Article

References (55)

1. Structural and functional properties of the evolutionarily ancient Y-box family of nucleic acid binding proteins. Wolffe AP, Bioessays 1994 16 245 251 10.1002/bies.950160407 8031301 (Pubitemid 2073505)
2. Induction of proteins in response to low temperature in Escherichia coli. Jones PG, VanBogelen RA, Neidhardt FC, J Bacteriol 1987 169 2092 2095 3553157 (Pubitemid 17081772)
3. Transcription factor YB-1 mediates DNA polymerase alpha gene expression. En-Nia A, Yilmaz E, Klinge U, Lovett DH, Stefanidis I, Mertens PR, J Biol Chem 2005 280 7702 7711 15615704 (Pubitemid 40349663)
4. YB-1 as a cell cycle-regulated transcription factor facilitating cyclin A and cyclin B1 gene expression. Jurchott K, Bergmann S, Stein U, Walther W, Janz M, Manni I, Piaggio G, Fietze E, Dietel M, Royer HD, J Biol Chem 2003 278 27988 27996 10.1074/jbc.M212966200 12695516 (Pubitemid 36899994)
5. Y-box factor YB1 controls p53 apoptotic function. Homer C, Knight DA, Hananeia L, Sheard P, Risk J, Lasham A, Royds JA, Braithwaite AW, Oncogene 2005 24 8314 8325 10.1038/sj.onc.1208998 16158057 (Pubitemid 43250923)
6. Y-box-binding protein YB-1 mediates transcriptional repression of human alpha 2(I) collagen gene expression by interferon-gamma. Higashi K, Inagaki Y, Suzuki N, Mitsui S, Mauviel A, Kaneko H, Nakatsuka I, J Biol Chem 2003 278 5156 5162 10.1074/jbc.M208724200 12446674 (Pubitemid 36801027)
7. Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Chen CY, Gherzi R, Andersen JS, Gaietta G, Jurchott K, Royer HD, Mann M, Karin M, Genes Dev 2000 14 1236 1248 10817758 (Pubitemid 30327504)
8. Cold shock domain factors activate the granulocyte-macrophage colony-stimulating factor promoter in stimulated jurkat T cells. Diamond P, Shannon MF, Vadas MA, Coles LS, J Biol Chem 2001 276 7943 7951 10.1074/jbc.M009836200 11116154
9. Characterization of the cDNA encoding a protein binding to the major histocompatibility complex class II Y box. Didier DK, Schiffenbauer J, Woulfe SL, Zacheis M, Schwartz BD, Proc Natl Acad Sci U S A 1988 85 7322 7326 10.1073/pnas.85.19.7322 3174636
10. Nuclear localization and increased levels of transcription factor YB-1 in primary human breast cancers are associated with intrinsic MDR1 gene expression. Bargou RC, Jurchott K, Wagener C, Bergmann S, Metzner S, Bommert K, Mapara MY, Winzer KJ, Dietel M, Dorken B, Royer HD, Nat Med 1997 3 447 450 10.1038/nm0497-447 9095180 (Pubitemid 27145688)
11. Glomerular mesangial cell-specific transactivation of matrix metalloproteinase 2 transcription is mediated by YB-1. Mertens PR, Harendza S, Pollock AS, Lovett DH, J Biol Chem 1997 272 22905 22912 10.1074/jbc.272.36.22905 9278454 (Pubitemid 27386113)
12. Y box-binding factor promotes eosinophil survival by stabilizing granulocyte-macrophage colony-stimulating factor mRNA. Capowski EE, Esnault S, Bhattacharya S, Malter JS, J Immunol 2001 167 5970 5976 11698476 (Pubitemid 33062794)
13. Posttranscriptional control of renin synthesis: identification of proteins interacting with renin mRNA 3′-untranslated region. Skalweit A, Doller A, Huth A, Kahne T, Persson PB, Thiele BJ, Circ Res 2003 92 419 427 10.1161/01.RES.0000059300.67152.4E 12600897 (Pubitemid 36298202)
14. Structural organization of mRNA complexes with major core mRNP protein YB-1. Skabkin MA, Kiselyova OI, Chernov KG, Sorokin AV, Dubrovin EV, Yaminsky IV, Vasiliev VD, Ovchinnikov LP, Nucleic Acids Res 2004 32 5621 5635 10.1093/nar/gkh889 15494450 (Pubitemid 39545678)
15. The major mRNA-associated protein YB-1 is a potent 5′ cap-dependent mRNA stabilizer. Evdokimova V, Ruzanov P, Imataka H, Raught B, Svitkin Y, Ovchinnikov LP, Sonenberg N, Embo J 2001 20 5491 5502 10.1093/emboj/20.19.5491 11574481 (Pubitemid 32959469)
16. Y-box protein-1 controls transforming growth factor-beta1 translation in proximal tubular cells. Fraser DJ, Phillips AO, Zhang X, van Roeyen CR, Muehlenberg P, En-Nia A, Mertens PR, Kidney international 2008 73 724 732 10.1038/sj.ki.5002719 18075498 (Pubitemid 351323248)
17. Splicing factor SRp30c interaction with Y-box protein-1 confers nuclear YB-1 shuttling and alternative splice site selection. Raffetseder U, Frye B, Rauen T, Jurchott K, Royer HD, Jansen PL, Mertens PR, J Biol Chem 2003 278 18241 18248 10.1074/jbc.M212518200 12604611 (Pubitemid 36799442)
18. Nucleocytoplasmic shuttling of transcription factors. Cartwright P, Helin K, Cell Mol Life Sci 2000 57 1193 1206 10.1007/PL00000759 11028912 (Pubitemid 30663477)
19. Hyperthermia-induced nuclear translocation of transcription factor YB-1 leads to enhanced expression of multidrug resistance-related ABC transporters. Stein U, Jurchott K, Walther W, Bergmann S, Schlag PM, Royer HD, J Biol Chem 2001 276 28562 28569 10.1074/jbc.M100311200 11369762
20. Role of the human Y box-binding protein YB-1 in cellular sensitivity to the DNA-damaging agents cisplatin, mitomycin C, and ultraviolet light. Ohga T, Koike K, Ono M, Makino Y, Itagaki Y, Tanimoto M, Kuwano M, Kohno K, Cancer Res 1996 56 4224 4228 8797596 (Pubitemid 26305020)
21. Transcriptional regulation of multidrug resistance-1 gene by interleukin-2 in lymphocytes. Tsujimura S, Saito K, Nakayamada S, Nakano K, Tsukada J, Kohno K, Tanaka Y, Genes Cells 2004 9 1265 1273 10.1111/j.1365-2443. 2004.00803.x 15569157 (Pubitemid 39618539)
22. Y-box protein-1 is the crucial mediator of antifibrotic interferon-gamma effects. Dooley S, Said HM, Gressner AM, Floege J, En-Nia A, Mertens PR, J Biol Chem 2006 281 1784 1795 16278212
23. Nuclear expression of Y-box-binding protein-1 correlates with P-glycoprotein and topoisomerase II alpha expression, and with poor prognosis in synovial sarcoma. Oda Y, Ohishi Y, Saito T, Hinoshita E, Uchiumi T, Kinukawa N, Iwamoto Y, Kohno K, Kuwano M, Tsuneyoshi M, J Pathol 2003 199 251 258 10.1002/path.1282 12533839 (Pubitemid 36176032)
24. Nuclear YB-1 expression as a negative prognostic marker in nonsmall cell lung cancer. Gessner C, Woischwill C, Schumacher A, Liebers U, Kuhn H, Stiehl P, Jurchott K, Royer HD, Witt C, Wolff G, Eur Respir J 2004 23 14 19 10.1183/09031936.03.00033203 14738225 (Pubitemid 38088490)
25. 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. Janz M, Harbeck N, Dettmar P, Berger U, Schmidt A, Jurchott K, Schmitt M, Royer HD, Int J Cancer 2002 97 278 282 10.1002/ijc.1610 11774277 (Pubitemid 34049016)
26. YB-1 is upregulated during prostate cancer tumor progression and increases P-glycoprotein activity. Gimenez-Bonafe P, Fedoruk MN, Whitmore TG, Akbari M, Ralph JL, Ettinger S, Gleave ME, Nelson CC, Prostate 2004 59 337 349 10.1002/pros.20023 15042610 (Pubitemid 38509767)
27. Constitutive rat multidrug-resistance protein 2 gene transcription is down-regulated by Y-box protein 1. Geier A, Mertens PR, Gerloff T, Dietrich CG, En-Nia A, Kullak-Ublick GA, Karpen SJ, Matern S, Gartung C, Biochem Biophys Res Commun 2003 309 612 618 10.1016/j.bbrc.2003.08.041 12963034 (Pubitemid 37083295)
28. PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Nakai K, Horton P, Trends Biochem Sci 1999 24 34 36 10.1016/S0968-0004(98)01336-X 10087920 (Pubitemid 29074461)
29. Inhibition of protein synthesis by Y box-binding protein 1 blocks oncogenic cell transformation. Bader AG, Vogt PK, Mol Cell Biol 2005 25 2095 2106 10.1128/MCB.25.6.2095-2106.2005 15743808 (Pubitemid 40354610)
30. Differential regulation of chemokine CCL5 expression in monocytes/macrophages and renal cells by Y-box protein-1. Raffetseder U, Rauen T, Djudjaj S, Kretzler M, En-Nia A, Tacke F, Zimmermann HW, Nelson PJ, Frye BC, Floege J, et al. Kidney international 2009 75 185 196 10.1038/ki.2008.457 18800033
31. NESbase version 1.0: a database of nuclear export signals. la Cour T, Gupta R, Rapacki K, Skriver K, Poulsen FM, Brunak S, Nucleic Acids Res 2003 31 393 396 10.1093/nar/gkg101 12520031 (Pubitemid 36150410)
32. Interaction of the universal mRNA-binding protein, p50, with actin: a possible link between mRNA and microfilaments. Ruzanov PV, Evdokimova VM, Korneeva NL, Hershey JW, Ovchinnikov LP, J Cell Sci 1999 112 Pt 20 3487 3496 10504297
33. Proteasome-mediated cleavage of the Y-box-binding protein 1 is linked to DNA-damage stress response. Sorokin AV, Selyutina AA, Skabkin MA, Guryanov SG, Nazimov IV, Richard C, Th'ng J, Yau J, Sorensen PH, Ovchinnikov LP, Evdokimova V, Embo J 2005 24 3602 3612 10.1038/sj.emboj.7600830 16193061 (Pubitemid 41509367)
34. Thrombin induces the release of the Y-box protein dbpB from mRNA: a mechanism of transcriptional activation. Stenina OI, Shaneyfelt KM, DiCorleto PE, Proc Natl Acad Sci U S A 2001 98 7277 7282 10.1073/pnas.121592298 11390977 (Pubitemid 32567939)
35. Tissue-specific enhancer-promoter interactions regulate high level constitutive expression of matrix metalloproteinase 2 by glomerular mesangial cells. Harendza S, Pollock AS, Mertens PR, Lovett DH, J Biol Chem 1995 270 18786 18796 10.1074/jbc.270.32.18786 7642529
36. A synergistic interaction of transcription factors AP2 and YB-1 regulates gelatinase a enhancer-dependent transcription. Mertens PR, Alfonso-Jaume MA, Steinmann K, Lovett DH, J Biol Chem 1998 273 32957 32965 10.1074/jbc.273.49. 32957 9830047 (Pubitemid 28557689)
37. The Y-box binding protein YB-1 suppresses collagen alpha 1(I) gene transcription via an evolutionarily conserved regulatory element in the proximal promoter. Norman JT, Lindahl GE, Shakib K, En-Nia A, Yilmaz E, Mertens PR, J Biol Chem 2001 276 29880 29890 10.1074/jbc.M103145200 11395503
38. Y box-binding protein-1 binds preferentially to single-stranded nucleic acids and exhibits 3′→5′ exonuclease activity. Izumi H, Imamura T, Nagatani G, Ise T, Murakami T, Uramoto H, Torigoe T, Ishiguchi H, Yoshida Y, Nomoto M, et al. Nucleic Acids Res 2001 29 1200 1207 10.1093/nar/29.5.1200 11222770 (Pubitemid 32186206)
39. Y-box protein 1 mediates PDGF-B effects in mesangioproliferative glomerular disease. van Roeyen CR, Eitner F, Martinkus S, Thieltges SR, Ostendorf T, Bokemeyer D, Luscher B, Luscher-Firzlaff JM, Floege J, Mertens PR, J Am Soc Nephrol 2005 16 2985 2996 10.1681/ASN.2004111009 16093451 (Pubitemid 44743496)
40. YB-1 acts as a ligand for notch-3 receptors and modulates receptor activation. Rauen T, Raffetseder U, Frye BC, Djudjaj S, Muhlenberg PJ, Eitner F, Lendahl U, Bernhagen J, Dooley S, Mertens PR, J Biol Chem 2009 284 26928 26940 10.1074/jbc.M109.046599 19640841
41. Y-box protein-1 is actively secreted through a non-classical pathway and acts as an extracellular mitogen. Frye BC, Halfter S, Djudjaj S, Muehlenberg P, Weber S, Raffetseder U, En-Nia A, Knott H, Baron JM, Dooley S, et al. EMBO reports 2009 10 783 789 10.1038/embor.2009.81 19483673
42. PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E, Murray B, Latham V, Sullivan M, Nucleic Acids Res 2012 40 261 D270 10.1093/nar/gkr1122 22135298
43. Proteasomal degradation of the multifunctional regulator YB-1 is mediated by an F-Box protein induced during programmed cell death. Lutz M, Wempe F, Bahr I, Zopf D, von Melchner H, FEBS letters 2006 580 3921 3930 10.1016/j.febslet. 2006.06.023 16797541 (Pubitemid 43946885)
44. Genotoxic stress-induced nuclear localization of oncoprotein YB-1 in the absence of proteolytic processing. Cohen SB, Ma W, Valova VA, Algie M, Harfoot R, Woolley AG, Robinson PJ, Braithwaite AW, Oncogene 2010 29 403 410 10.1038/onc.2009.321 19838214
45. Prognostic association of YB-1 expression in breast cancers: a matter of antibody. Woolley AG, Algie M, Samuel W, Harfoot R, Wiles A, Hung NA, Tan PH, Hains P, Valova VA, Huschtscha L, et al. PLoS One 2011 6 20603 10.1371/journal.pone.0020603 21695211
46. Binding of Y-box proteins to RNA: involvement of different protein domains. Ladomery M, Sommerville J, Nucleic Acids Res 1994 22 5582 5589 10.1093/nar/22.25.5582 7530842
47. Masking of mRNA by Y-box proteins. Sommerville J, Ladomery M, FASEB J 1996 10 435 443 8647342 (Pubitemid 26120318)
48. Identification of Y-box binding protein 1 as a core regulator of MEK/ERK pathway-dependent gene signatures in colorectal cancer cells. Jurchott K, Kuban RJ, Krech T, Bluthgen N, Stein U, Walther W, Friese C, Kielbasa SM, Ungethum U, Lund P, et al. PLoS Genet 2010 6 1001231 10.1371/journal.pgen.1001231 21170361
49. YB-1: oncoprotein, prognostic marker and therapeutic target? Lasham A, Print CG, Woolley AG, Dunn SE, Braithwaite AW, Biochem J 2013 449 11 23 10.1042/BJ20121323 23216250
50. The proteasome inhibitor bortezomib depletes plasma cells and protects mice with lupus-like disease from nephritis. Neubert K, Meister S, Moser K, Weisel F, Maseda D, Amann K, Wiethe C, Winkler TH, Kalden JR, Manz RA, Voll RE, Nat Med 2008 14 748 755 10.1038/nm1763 18542049 (Pubitemid 351951516)
51. Myeloperoxidase-specific plasma cell depletion by bortezomib protects from anti-neutrophil cytoplasmic autoantibodies-induced glomerulonephritis. Bontscho J, Schreiber A, Manz RA, Schneider W, Luft FC, Kettritz R, J Am Soc Nephrol 2011 22 336 348 10.1681/ASN.2010010034 21233415
52. Pressure oscillation regulates human mesangial cell growth and collagen synthesis. Mertens PR, Espenkott V, Venjakob B, Heintz B, Handt S, Sieberth HG, Hypertension 1998 32 945 952 10.1161/01.HYP.32.5.945 9822458 (Pubitemid 28530233)
53. Transcription factor Ets-1 regulates gelatinase a gene expression in mesangial cells. Reisdorff J, En-Nia A, Stefanidis I, Floege J, Lovett DH, Mertens PR, J Am Soc Nephrol 2002 13 1568 1578 10.1097/01.ASN.0000015617.39974. FB 12039986 (Pubitemid 34579246)
54. YB-1 regulation of the human and rat gelatinase A genes via similar enhancer elements. Mertens PR, Alfonso-Jaume MA, Steinmann K, Lovett DH, J Am Soc Nephrol 1999 10 2480 2487 10589685
55. Y-box binding protein-1 mediates profibrotic effects of calcineurin inhibitors in the kidney. Hanssen L, Frye BC, Ostendorf T, Alidousty C, Djudjaj S, Boor P, Rauen T, Floege J, Mertens PR, Raffetseder U, J Immunol 2011 187 298 308 10.4049/jimmunol.1100382 21606250