Navegar

Colección

Datos Estadísticas

Artículo

Degese, M.S.; Tanos, T.; Naipauer, J.; Gingerich, T.; Chiappe, D.; Echeverria, P.; LaMarre, J.; Gutkind, J.S.; Coso, O.A. "An interplay between the p38 MAPK pathway and AUBPs regulates c-fos mRNA stability during mitogenic stimulation" (2015) Biochemical Journal. 467(1):77-90
El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Mitogen-activated protein kinase (MAPK) pathways constitute key regulatory elements linking extracellular stimuli to nuclear gene expression. Immediate-early responsive genes (IEGs) of the activator protein 1 (AP-1) family, such as fos, achieve peak expression levels shortly after cells are stimulated with growth factors and sharply decrease thereafter. Several AU-rich binding proteins (AUBPs), including HuR (Hu-antigen R, Elavlike protein 1, ELAVL1) and KSRP (far upstream element-binding protein 2, KHSRP) bind to a fos AU-rich element (ARE) present in the 3′-UTR (untranslated region) of fos mRNA regulating its stability by a still poorly defined mechanism. We show in the present study that, whereas HuR binds and stabilizes transcribed reporter mRNAs bearing the fos 3′-UTR, KSRP counteracts this effect. Furthermore, we found that fos mRNA stability and HuR phosphorylation status are dependent on the activity of p38 MAPK in both epithelial cells and fibroblasts upon proliferative stimulation. Analysing PPI (protein-protein interaction) networks, we performed a thorough query of interacting proteins for p38 MAPKs, HuR and other AUBPs upon growth factor stimulation. This revealed novel HuR interactors including inhibitors of protein phosphatase 2 (PP2A) activity. Over-expression of two of these interactors, pp32 and APRIL (acidic leucine-rich nuclear phosphoprotein 32 family member B, ANP32B) and pharmacological inhibition of PP2A stabilized a fos reporter mRNA. Our results indicate that p38 MAPK regulates fos mRNA decay by affecting the state of phosphorylation of HuR while controlling yet to be fully elucidated PP regulatory networks. © The Authors Journal compilation © 2015 Biochemical Society.

Registro:

Documento: Artículo
Título:An interplay between the p38 MAPK pathway and AUBPs regulates c-fos mRNA stability during mitogenic stimulation
Autor:Degese, M.S.; Tanos, T.; Naipauer, J.; Gingerich, T.; Chiappe, D.; Echeverria, P.; LaMarre, J.; Gutkind, J.S.; Coso, O.A.
Filiación:LFBM-DFBMC, Departamento de Fisiología Y Biología Molecular, Universidad de Buenos Aires (FCEN-UBA), Buenos Aires, C1428EHA, Argentina
IFIBYNE-CONICET, Buenos Aires, C1428EHA, Argentina
DBMS, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada
Proteomics Core Facility, École Polytechnique Fédérale de Lausanne, Lausanne, CH-1015, Switzerland
Département de Biologie Cellulaire, Université de Genève, Sciences 3, Genève 4, CH-1211, Switzerland
Oral and Pharyngeal Cancer Branch, National Institute of Dental and Craniofacial Research, NIH, Bethesda, MD 20892-4330, United States
Palabras clave:AUBPs.; C-fos; P38 MAPKs; Stability of mRNAs; acidic leucine rich nuclear phosphoprotein 32 family member B; AU rich binding protein; binding protein; far upstream element binding protein 2; Hu antigen; Hu antigen R; messenger RNA; mitogen activated protein kinase p38; phosphoprotein; phosphoprotein phosphatase 2; protein c fos; unclassified drug; 3' untranslated region; ELAVL1 protein, human; Hu antigen; hybrid protein; KHSRP protein, human; KSRP protein, mouse; messenger RNA; mitogen activated protein kinase p38; mitogenic agent; protein c fos; protein kinase inhibitor; RNA binding protein; transactivator protein; 3' untranslated region; Article; cell proliferation; controlled study; embryo; enzyme activity; epithelium cell; fibroblast; gene overexpression; human; human cell; mitogenesis; priority journal; protein function; protein phosphorylation; protein protein interaction; protein RNA binding; RNA stability; 3T3 cell line; animal; chemistry; comparative study; drug effects; genetics; HEK293 cell line; HeLa cell line; metabolism; mouse; mutation; phosphorylation; protein processing; RNA stability; signal transduction; 3' Untranslated Regions; Animals; Cell Proliferation; HEK293 Cells; HeLa Cells; Hu Paraneoplastic Encephalomyelitis Antigens; Humans; MAP Kinase Signaling System; Mice; Mitogens; Mutation; NIH 3T3 Cells; p38 Mitogen-Activated Protein Kinases; Phosphorylation; Protein Kinase Inhibitors; Protein Processing, Post-Translational; Proto-Oncogene Proteins c-fos; Recombinant Fusion Proteins; RNA Stability; RNA, Messenger; RNA-Binding Proteins; Trans-Activators
Año:2015
Volumen:467
Número:1
Página de inicio:77
Página de fin:90
DOI: http://dx.doi.org/10.1042/BJ20141100
Título revista:Biochemical Journal
Título revista abreviado:Biochem. J.
ISSN:02646021
CODEN:BIJOA
CAS:3' Untranslated Regions; ELAVL1 protein, human; Hu Paraneoplastic Encephalomyelitis Antigens; KHSRP protein, human; KSRP protein, mouse; Mitogens; p38 Mitogen-Activated Protein Kinases; Protein Kinase Inhibitors; Proto-Oncogene Proteins c-fos; Recombinant Fusion Proteins; RNA, Messenger; RNA-Binding Proteins; Trans-Activators
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02646021_v467_n1_p77_Degese

Referencias:

  • Tanos, T., Marinissen, M.J., Coluccio-Leskow, F., Hochbaum, D., Martinetto, H., Gutkind, J.S., Coso, O.A., Phosphorylation of c-Fos by members of the p38 MAPK family. Role in the AP-1 response to UV light (2005) J. Biol. Chem., 280, pp. 18842-18852. , CrossRef PubMed
  • Cochran, B.H., Zullo, J., Verma, I.M., Stiles, C.D., Expression of the c-fos gene and of a fos-related gene is stimulated by platelet-derived growth factor (1984) Science, 226, pp. 1080-1082. , CrossRef PubMed
  • Coso, O.A., Chiarello, M., Kalinec, G., Kyriakis, J.M., Woodgett, J., Gutkind, J.S., Transforming G protein-coupled receptors potently activate JNK (SAPK). Evidence for a divergence from the tyrosine kinase signaling pathway (1995) J. Biol. Chem., 270, pp. 5620-5624. , CrossRef PubMed
  • Monje, P., Marinissen, M.J., Gutkind, J.S., Phosphorylation of the carboxyl-terminal transactivation domain of c-Fos by extracellular signal-regulated kinase mediates the transcriptional activation of AP-1 and cellular transformation induced by platelet-derived growth factor (2003) Mol. Cell. Biol., 23, pp. 7030-7043. , CrossRef PubMed
  • Yang, S.H., Sharrocks, A.D., Whitmarsh, A.J., Transcriptional regulation by the MAP kinase signaling cascades (2003) Gene, 320, pp. 3-21. , CrossRef PubMed
  • O'Donnell, A., Odrowaz, Z., Sharrocks, A.D., Immediate-early gene activation by the MAPK pathways: What do and don't we know? (2012) Biochem. Soc. Trans., 40, pp. 58-66. , CrossRef PubMed
  • Gingerich, T.J., Feige, J.J., LaMarre, J., AU-rich elements and the control of gene expression through regulated mRNA stability (2004) Anim. Health Res. Rev., 5, pp. 49-63. , CrossRef PubMed
  • Barreau, C., Paillard, L., Osborne, B., AU-rich elements and associated factors: Are there unifying principles? (2006) Nucleic Acids Res., 33, pp. 7138-7150. , CrossRef PubMed
  • Shyu, A.B., Greenberg, M.E., Belasco, J.G., The c-fos transcript is targeted for rapid decay by two distinct mRNA degradation pathways (1989) Genes Dev., 3, pp. 60-72. , CrossRef PubMed
  • Chen, C.A., Xu, N., Shyu, A.B., mRNA decay mediated by two distinct AU-rich elements from c-fos and granulocyte-macrophage colony-stimulating factor transcripts: Different deadenylation kinetics and uncoupling from translation (1995) Mol. Cell. Biol., 15, pp. 5777-5788. , PubMed
  • Ma, W.J., Cheng, S., Campbell, C., Wright, A., Furneaux, H., Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein (1996) J. Biol. Chem., 271, pp. 8144-8151. , CrossRef PubMed
  • Kajita, Y., Nakayama, J., Aizawa, M., Ishikawa, F., The UUAG-specific RNA binding protein, heterogeneous nuclear ribonucleoprotein D0. Common modular structure and binding properties of the 2xRBD-Gly family (1995) J. Biol. Chem., 270, pp. 22167-22175. , CrossRef PubMed
  • Chou, C.F., Mulky, A., Maitra, S., Lin, W.J., Gherzi, R., Kappes, J., Chen, C.Y., Tethering KSRP, a decay-promoting AU-rich element-binding protein, to mRNAs elicits mRNA decay (2006) Mol. Cell. Biol., 26, pp. 3695-3706. , CrossRef PubMed
  • Carballo, E., Lai, W.S., Blackshear, P.J., Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin (1998) Science, 281, pp. 1001-1005. , CrossRef PubMed
  • Stoecklin, G., Colombi, M., Reineri, I., Leuenberger, S.A., Mallaun, M., Schmidlin, M., Gross, B., Moroni, C., Functional cloning of BRF1, a regulator of ARE-dependent mRNA turnover (2002) EMBO J., 21, pp. 4709-4718. , CrossRef PubMed
  • Chen, C.Y., Gherzi, R., Ong, S.E., Chan, E.L., Raijmakers, R., Prujin, G.J.M., Stoecklin, G., Karin, M., AU binding proteins recruit the exosome to degrade ARE-containing mRNAs (2001) Cell, 107, pp. 451-464. , CrossRef PubMed
  • Zhu, W., Brauchle, M.A., Di Padova, F., Gram, H., New, L., Ono, K., Downey, J.S., Han, J., Gene suppression by tristetraprolin and release by the p38 pathway (2001) Am. J. Physiol. Lung Cell. Mol. Physiol., 281, pp. L499-L508. , PubMed
  • Stoecklin, G., Stubbs, T., Kedersha, N., Wax, S., Rigby, W.F.C., Blackwell, T.K., Anderson, P., MK2-induced tristetraprolin:14-3-3 complexes prevent stress granule association and ARE-mRNA decay (2004) EMBO J., 23, pp. 1313-1324. , CrossRef PubMed
  • Mahtani, K.R., Brook, M., Dean, J.L.E., Sully, G., Saklatvala, J., Clark, A.R., Mitogen-activated protein kinase p38 controls the expression and posttranslational modification of tristetraprolin, a regulator of tumor necrosis factor alpha mRNA stability (2001) Mol. Cell. Biol., 21, pp. 6461-6469. , CrossRef PubMed
  • Chen, C.A., Xu, N., Shyu, A.B., Highly selective actions of HuR in antagonizing AU-rich element-mediated mRNA destabilization (2002) Mol. Cell. Biol., 22, pp. 7268-7278. , CrossRef PubMed
  • Abdelmohsen, K., Pullman, R., Lal, A., Kim, H.H., Galban, S., Yang, X., Beltrow, J.D., Gillespie, D.A., Phosphorylation of HuR by Chk2 regulates SIRT1 expression (2007) Mol. Cell, 25, pp. 543-557. , CrossRef PubMed
  • Kim, H.H., Abdelmohsen, K., Lal, A., Pullman, R., Yang, X., Galban, S., Srikantan, S., Gorospe, M., Nuclear HuR accumulation through phosphorylation by Cdk1 (2008) Genes Dev., 22, pp. 1804-1815. , CrossRef PubMed
  • Doller, A., Winkler, C., Azrilian, I., Schulz, S., Hartman, S., Pfeilsschifter, J., Eberhardt, W., High-constitutive HuR phosphorylation at Ser 318 by PKC{delta} propagates tumor relevant functions in colon carcinoma cells (2011) Carcinogenesis, 32, pp. 676-685. , CrossRef PubMed
  • Lafarga, V., Cuadrado, A., Lopez De Silanes, I., Bengochea, R., Fernandez-Capetillo, O., Nebreda, A.R., p38 Mitogen-activated protein kinase- and HuR-dependent stabilization of p21(Cip1) mRNA mediates the G(1)S checkpoint (2009) Mol. Cell. Biol., 29, pp. 4341-4351. , CrossRef PubMed
  • Linker, K., Pautz, A., Fechir, M., Hubrich, T., Greeve, J., Kleinert, H., Involvement of KSRP in the post-transcriptional regulation of human iNOS expression-complex interplay of KSRP with TTP and HuR (2005) Nucleic Acids Res., 33, pp. 4813-4827. , CrossRef PubMed
  • Gallouzi, I., Brennan, C.M., Steitz, J.A., Protein ligands mediate the CRM1-dependent export of HuR in response to heat shock (2001) RNA, 7, pp. 1348-1361. , CrossRef PubMed
  • Naipauer, J., Gatelli, A., Degese, M., Slomiansky, V., Werthmeier, E., LaMarre, J., Castilla, L., Coso, O.A., The use of alternative polyadenylation sites renders integrin β1 (Itgb1) mRNA isoforms with differential stability during mammary gland development (2013) Biochem. J., 454, pp. 345-357. , CrossRef PubMed
  • You, Y., Chen, C.A., Shyu, A.B., Two cellular proteins bind specifically to a purine-rich sequence necessary for the destabilization function of a c-fos protein-coding region determinant of mRNA instability (1992) Mol. Cell. Biol., 12, pp. 2931-2940. , PubMed
  • Echeverria, P.C., Forafonov, F., Pandey, D.P., Mulebach, G., Picard, D., Detection of changes in gene regulatory patterns, elicited by perturbations of the Hsp90 molecular chaperone complex, by visualizing multiple experiments with an animation (2011) BioData Min., 4, p. 15. , CrossRef PubMed
  • Cline, M., Smoot, M., Cerami, E., Kuchinsky, A., Landys, N., Workman, C., Christmas, R., Gross, B., Integration of biological networks and gene expression data using cytoscape (2007) Nat. Protoc., 2, pp. 2366-2382. , CrossRef PubMed
  • Echeverria, P.C., Bernthaler, A., Dupuis, P., Mayer, B., Picard, D., An interaction network predicted from public data as a discovery tool: Application to the Hsp90 molecular chaperone machine (2011) PLoS One, 6. , CrossRef PubMed
  • Briata, P., Forcales, S.P., Ponassi, M., Corte, G., Chen, C.Y., Karin, M., Puri, P.L., Gherzi, R., p38-dependent phosphorylation of the mRNA decay-promoting factor KSRP controls the stability of select myogenic transcripts (2005) Mol. Cell, 20, pp. 891-903. , CrossRef PubMed
  • Brennan, C.M., Gallouzi, I., Steitz, J.A., Protein ligands to HuR modulate its interaction with target mRNAs in vivo (2000) J.CellBiol., 151, pp. 1-13. , CrossRef PubMed
  • Fromm, C., Coso, O.A., Montaner, S., Xu, N., Gutkind, J.S., The small GTP-binding protein Rho links G protein-coupled receptors and Galpha12 to the serum response element and to cellular transformation (1997) Proc. Natl. Acad. Sci. U.S.A., 94, pp. 10098-10103. , CrossRef PubMed
  • Spitz, F., Furlong, E., Transcription factors: From enhancer binding to developmental control (2012) Nat. Rev. Genet., 13, pp. 613-626. , CrossRef PubMed
  • Johnson, D., Dent, S., Chromatin: Receiver and quarterback for cellular signals (2013) Cell, 152, pp. 685-689. , CrossRef PubMed
  • Otkjaer, K., Holtman, H., Kragstrup, T.W., Paludan, S.R., Johansen, C., Gaesthel, M., Kragballe, K., Iversen, L., The p38 MAPK regulates IL-24 expression by stabilization of the 3′ UTR of IL-24 mRNA (2010) PLoS One, 5. , CrossRef PubMed
  • Winzen, R., Kracht, M., Ritter, B., Wilhem, A., Chen, C.A., Shyu, A.B., Muller, M., Holtmann, H., The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism (1999) EMBO J., 18, pp. 4969-4980. , CrossRef PubMed
  • Hitti, E., Iakovleva, T., Brook, M., Deppenmeier, S., Gruber, A.D., Radzioch, D., Clark, A.R., Gaesthel, M., Mitogen-activated protein kinase-activated protein kinase 2 regulates tumor necrosis factor mRNA stability and translation mainly by altering tristetraprolin expression, stability, and binding to adenineuridine-rich element (2006) Mol. Cell. Biol., 26, pp. 2399-2407. , CrossRef PubMed
  • Frevel, M.A.E., Bakheet, T., Silva, A.M., Hissong, J.G., Khabar, K.S.A., Williams, B.R.G., p38 Mitogen-activated protein kinase-dependent and -independent signaling of mRNA stability of AU-rich element-containing transcripts (2003) Mol. Cell. Biol., 23, pp. 425-436. , CrossRef PubMed
  • Fan, X.C., Steitz, J.A., Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs (1998) EMBO J., 17, pp. 3448-3460. , CrossRef PubMed
  • Lopez De Silanes, I., Lal, A., Gorospe, M., HuR: Post-transcriptional paths to malignancy (2005) RNA Biol., 2, pp. 11-13. , CrossRef PubMed
  • Eberhardt, W., Doller, A., Pfeilsschifter, J., Regulation of the mRNA-binding protein HuR by posttranslational modification: Spotlight on phosphorylation (2012) Curr. Protein Pept. Sci., 13, pp. 380-390. , CrossRef PubMed
  • Doller, A., Schlepckow, K., Schwalbe, H., Pfeilsschifter, J., Eberhardt, W., Tandem phosphorylation of serines 221 and 318 by protein kinase Cdelta coordinates mRNA binding and nucleocytoplasmic shuttling of HuR (2010) Mol. Cell. Biol., 30, pp. 1397-1410. , CrossRef PubMed
  • Tiedje, C., Ronkina, N., Tehrani, M., Dhamija, S., Laass, K., Holtmann, H., Kotlyarov, A., Gaesthel, M., The p38MK2-driven exchange between tristetraprolin and HuR regulates AU-rich element-dependent translation (2012) PLoS Genet., 8. , CrossRef PubMed

Citas:

---------- APA ----------
Degese, M.S., Tanos, T., Naipauer, J., Gingerich, T., Chiappe, D., Echeverria, P., LaMarre, J.,..., Coso, O.A. (2015) . An interplay between the p38 MAPK pathway and AUBPs regulates c-fos mRNA stability during mitogenic stimulation. Biochemical Journal, 467(1), 77-90.
http://dx.doi.org/10.1042/BJ20141100
---------- CHICAGO ----------
Degese, M.S., Tanos, T., Naipauer, J., Gingerich, T., Chiappe, D., Echeverria, P., et al. "An interplay between the p38 MAPK pathway and AUBPs regulates c-fos mRNA stability during mitogenic stimulation" . Biochemical Journal 467, no. 1 (2015) : 77-90.
http://dx.doi.org/10.1042/BJ20141100
---------- MLA ----------
Degese, M.S., Tanos, T., Naipauer, J., Gingerich, T., Chiappe, D., Echeverria, P., et al. "An interplay between the p38 MAPK pathway and AUBPs regulates c-fos mRNA stability during mitogenic stimulation" . Biochemical Journal, vol. 467, no. 1, 2015, pp. 77-90.
http://dx.doi.org/10.1042/BJ20141100
---------- VANCOUVER ----------
Degese, M.S., Tanos, T., Naipauer, J., Gingerich, T., Chiappe, D., Echeverria, P., et al. An interplay between the p38 MAPK pathway and AUBPs regulates c-fos mRNA stability during mitogenic stimulation. Biochem. J. 2015;467(1):77-90.
http://dx.doi.org/10.1042/BJ20141100