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Abstract:

Extracellular signal-regulated protein kinase 1 and 2 (ERK1/2) are members of the MAPK family and participate in the transduction of stimuli in cellular responses. Their long-term actions are accomplished by promoting the expression of specific genes whereas faster responses are achieved by direct phosphorylation of downstream effectors located throughout the cell. In this study we determined that hERK1 translocates to the mitochondria of HeLa cells upon a proliferative stimulus. In the mitochondrial environment, hERK1 physically associates with (i) at least 5 mitochondrial proteins with functions related to transport (i.e. VDAC1), signalling, and metabolism; (ii) histones H2A and H4; and (iii) other cytosolic proteins. This work indicates for the first time the presence of diverse ERK-complexes in mitochondria and thus provides a new perspective for assessing the functions of ERK1 in the regulation of cellular signalling and trafficking in HeLa cells. © 2009 Galli et al.

Registro:

Documento: Artículo
Título:A new paradigm for MAPK: Structural interactions of hERK1 with mitochondria in HeLa cells
Autor:Galli, S.; Jahn, O.; Hitt, R.; Hesse, D.; Opitz, L.; Plessmann, U.; Urlaub, H.; Poderoso, J.J.; Jares-Erijman, E.A.; Jovin, T.M.
Filiación:Laboratory of Cellular Dynamics, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
Departamento de Química Orgánica, Facultad de Ciencias Exactas y Naturales (FCEyN), Universidad de Buenos Aires (UBA), Buenos Aires, Argentina
Proteomics Group, Max Planck Institute of Experimental Medicine, Göttingen, Germany
Deutsche Forschungsgemeinschaft Research Center for Molecular Physiology of the Brain, Göttingen, Germany
Transkriptomanalyselabor, University of Göttingen, Department of Biochemistry and Molecular Cell Biology, Göttingen, Germany
Bioanalytical Mass Spectrometry Group, Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
Laboratory of Oxygen Metabolism, University Hospital Jose de San Martin, UBA, Buenos Aires, Argentina
Laboratorio Max Planck de Dinámica Celular, FCEyN, UBA, Buenos Aires, Argentina
Palabras clave:histone H2A; histone H4; mitogen activated protein kinase 1; mitogen activated protein kinase 3; voltage dependent anion channel; glutathione transferase; mitogen activated protein kinase 3; article; complex formation; controlled study; enzyme activity; gene control; gene expression; gene location; HeLa cell; human; human cell; mitochondrion; nucleotide sequence; protein protein interaction; protein transport; signal transduction; amino acid sequence; cell proliferation; gene expression profiling; gene expression regulation; mass spectrometry; metabolism; methodology; molecular genetics; proteomics; sequence homology; Amino Acid Sequence; Cell Proliferation; Gene Expression Profiling; Gene Expression Regulation, Enzymologic; Gene Expression Regulation, Neoplastic; Glutathione Transferase; Hela Cells; Humans; MAP Kinase Signaling System; Mitochondria; Mitogen-Activated Protein Kinase 3; Molecular Sequence Data; Proteomics; Sequence Homology, Amino Acid; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
Año:2009
Volumen:4
Número:10
DOI: http://dx.doi.org/10.1371/journal.pone.0007541
Título revista:PLoS ONE
Título revista abreviado:PLoS ONE
ISSN:19326203
CAS:mitogen activated protein kinase 1, 137632-08-7; mitogen activated protein kinase 3, 137632-07-6; glutathione transferase, 50812-37-8; Glutathione Transferase, 2.5.1.18; Mitogen-Activated Protein Kinase 3, 2.7.11.24
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_19326203_v4_n10_p_Galli.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19326203_v4_n10_p_Galli

Referencias:

  • Robinson, M.J., Cobb, M.H., Mitogen-activated protein kinase pathways (1997) Curr Opin Cell Biol, 9, pp. 180-186
  • Roux, P., Blenis, J., ERK and p38 MAPK-activated protein kinases: A family of protein kinases with diverse biological functions (2004) Microbiol Mol Biol Rev, 68, pp. 320-344
  • Yoon, S., Seger, R., The extracellular signal-regulated kinase: Multiple substrates regulate diverse cellular functions (2006) Growth Factors, 24, pp. 21-44
  • Shaul, Y.D., Seger, R., ERK1c regulates Golgi fragmentation during mitosis (2006) J Cell Biol, 172, pp. 885-897
  • Poderoso, C., Converso, D., Maloberti, P., Duarte, A., Neuman, I., A mitocondrial kinase complex is essential to mediate an ERK1/2 phosphorylation of a key regulatory protein in steroid biosynthesis (2008) PLoS One, 3, pp. e1443. , doi:10.1371/Journal.pone.0001443
  • Chen, R.H., Sarnecki, C., Blenis, J., Nuclear localization and regulation of erk- and rsk-encoded protein kinases (1992) Mol Cell Biol, 12, pp. 915-927
  • Lenormand P, Sardet C, Pages G, L'Allemain G, Brunet A, et al. (1993) Growth factors induce nuclear translocation of MAP kinases (p42mapk and p44mapk) but not of their activator MAP kinase kinase (p45mapkk) in fibroblasts. J Cell Biol 122: 1079-1088; Lloyd, A.C., Distinct functions for ERKs? (2006) J Biol, 5, p. 13
  • Klemke, R.L., Cai, S., Giannini, A.L., Gallagher, P.J., de Lanerolle, P., Regulation of cell motility by mitogen-activated protein kinase (1997) J Cell Biol, 137, pp. 481-492
  • Alonso, M., Melani, M., Converso, D., Jaitovich, A., Paz, C., Mitochondrial extracellular signal-regulated kinases 1/2 (ERK1/2) are modulated during brain development (2004) J Neurochem, 89, pp. 248-256
  • Baines, C.P., Zhang, J., Wan, G.W., Zheng, Y.T., Xiu, J.X., Mitochondrial PKCe and MAPK form signaling modules in the murine heart: Enhanced mitochondrial PKCe-MAPK interactions and differential MAPK activation in PKCe-induced cardioprotection (2002) Circ Res, 90, pp. 390-397
  • Galli, S., Antico Arciuch, V., Poderoso, C., Converso, P., Qiongqiong, Z., Tumor cell phenotype is sustained by selective MAPK oxidation in mitochondria (2008) PLoS One, 3, pp. e2379. , doi:10.1371/journal.pone0002379
  • Khokhlatchev, A.V., Canagarajah, B., Wilsbacher, J., Robinson, M., Atkinson, M., Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation (1998) Cell, 93, pp. 605-615
  • Canagarajah, B., Khokhlatchev, A.V., Cobb, M.H., Goldsmith, E., Activation mechanism of the MAP kinase ERK2 by dual phosphorylation (1997) Cell, 90, pp. 859-869
  • Cobb, M.H., Goldsmith, E., Dimerization in MAP-kinase signalling (2000) Trends Biochem Sci, 25, pp. 7-9
  • English, J., Pearson, G., Wilsbacher, J., Swantek, J., Karandikar, M., New insights into the control of MAP kinase pathways (1999) Exp Cell Res, 253, pp. 255-270
  • Casar, B., Pinto, A., Crespo, P., Essential role of ERK dimers in the activation of cytoplasmic but not nuclear substrates by ERK-scaffold complexes (2008) Mol Cell, 31, pp. 708-721
  • Philipova, R., Whitaker, M., Active ERK1 is dimerized in vivo: Bisphosphodimers generate peak kinase activity and monophosphodimers maintain basal ERK1 activity (2005) J Cell Sci, 118, pp. 5767-5776
  • Attardi, G., Schatz, G., Biogenesis of mitochondria (1988) Annu Rev Cell Biol, 4, pp. 289-333
  • Furuno, T., Hirashima, N., Onizawa, S., Sagiya, N., Nakanishi, M., Nuclear shuttling of mitogen-activated protein (MAP) kinase (extracellular signal-regulated kinase (ERK 2) was dynamically controlled by MAP/ERK kinase after antigen stimulation in RBL-2H3 cells (2001) J Immunol, 166, pp. 4416-4421
  • Costes, S., Daelemans, D., Cho, E., Dobbin, Z., Pavlakis, G., Automatic and quantitative measurement of protein-protein colocalization in live cells (2004) Biophys J, 86, pp. 3993-4003
  • Colombini, M., VDAC: The channel at the interface between mitochondria and the cytosol (2004) Mol Cell Biochem, 256-257 (1-2), pp. 107-115
  • Shoshan-Barmatz, V., Israelson, A., Brdiczka, D., Sheu, S.S., The voltage-dependent anion channel (VDAC): Function in intracellular signalling, cell life and cell death (2006) Curr Pharm Des, 12, pp. 2249-2270
  • Rostovtseva, T.K., Liu, T.T., Colombini, M., Parsegian, V.A., Bezrukov, S.M., Positive cooperativity without domains or subunits in a monomeric membrane channel (2000) Proc Natl Acad Sci USA, 97, pp. 7819-7822
  • Linden, M., Gellerfors, P., Hydrodynamic properties of porin isolated from outer membranes of rat liver mitochondria (1983) Biochim Biophys Acta, 736, pp. 125-129
  • Zalk, R., Israelson, A., Garty, E.S., Azoulay-Zohar, H., Shoshan-Barmatz, V., Oligomeric states of the voltage-dependent anion channel and cytochrome c release from mitochondria (2005) Biochem J, 386, pp. 73-78
  • Shi, Y., Jiang, C., Chen, Q., Tang, H., One-step on-column affinity refolding purification and functional analysis of recombinant human VDAC1 (2003) Biochem Biophys Res Commun, 303, pp. 475-482
  • Shoshan-Barmatz, V., Gincel, D., The voltage-dependent anion channel: Characterization, modulation, and role in mitochondrial function in cell life and death (2003) Cell Biochem Biophys, 39, pp. 279-292
  • Crompton, M., The mitochondrial permeability transition pore and its role in cell death (1999) Biochem J, 341, pp. 233-249
  • Bernardi, P., Mitochondrial transport of cations: Channels, exchangers, and permeability transition (1999) Physiol Rev, 79, pp. 1127-1155
  • Davis, R.J., The mitogen-activated protein kinase signal transduction pathway (1993) J Biol Chem, 268, pp. 14553-14556
  • Zhou, T., Sun, L., Humphreys, J., Goldsmith, E., Docking interactions induce exposure of activation loop in the MAP kinase ERK2 (2006) Structure, 14, pp. 1011-1019
  • Pearson, G., Robinson, F., Beers Gibson, T., Xu, B., Karandikar, M., Mitogen-activated protein (MAP) kinase pathways:regulation and physiological functions (2001) Endocrine Reviews, 22, pp. 153-183
  • Tanoue, T., Maeda, R., Adachi, M., Nishida, E., Identification of a docking groove on ERK and p38 MAP kinases that regulates the specificity of docking interactions (2001) EMBO J, 20, pp. 466-479
  • Tanoue, T., Adachi, M., Moriguchi, T., Nishida, E., A conserved docking motif in MAP kinases common substrates, activators and regulators (2000) Nat Cell Biol, 2, pp. 110-116
  • Enriquez, J.A., Fernandez-Silva, P., Perez-Martos, A., Lopez-Perez, M.J., Montoya, J., The synthesis of mRNA in isolated mitochondria can be maintained for several hours and is inhibited by high levels of ATP (1996) Eur J Biochem, 237, pp. 601-610
  • Roth, S.Y., Denu, J.M., Allis, C.D., Histone acetyltransferases (2001) Annu Rev Biochem, 70, pp. 81-120
  • Fink, M., Imholz, D., Thoma, F., Contribution of the serine 129 of histone H2A to chromatin structure (2007) Mol Cell Biol, 27, pp. 3589-3600
  • Okamura, H., Yoshida, K., Rabelo Amorim, B., Haneji, T., Histone H1.2 is translocated to mitochondria and associates with Bak in bleomycin-induced apoptotic cells (2008) J Cell Biochem, 103, pp. 1488-1496
  • Konishi, A., Shimizu, S., Hirota, J., Takao, T., Fan, Y., Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks (2003) Cell, 114, pp. 673-688
  • Schwertz, H., Carter, J.M., Abdudureheman, M., Russ, M., Buerke, U., Myocardial ischemia/reperfusion causes VDAC phosphorylation which is reduced by cardioprotection with a p38 MAP kinase inhibitor (2007) Proteomics, 7, pp. 4579-4588
  • Shadel, G.S., Clayton, D.A., Mitochondrial DNA maintenance in vertebrates (1997) Annu Rev Biochem, 66, pp. 409-435
  • Maniura-Weber, K., Goffart, S., Garstka, H.L., Montoya, J., Wiesner, R.J., Transient overexpression of mitochondrial transcription factor A (TFAM) is sufficient to stimulate mitochondrial DNA transcription, but not sufficient to increase mtDNA copy number in cultured cells (2004) Nucleic Acids Res, 32, pp. 6015-6027
  • Garstka, H.L., Schmitt, W.E., Schultz, J., Sogl, B., Silakowski, B., Import of mitochondrial transcription factor A (TFAM) into rat liver mitochondria stimulates transcription of mitochondrial DNA (2003) Nucleic Acids Res, 31, pp. 5039-5047
  • Kannan, N., Taylor, S., Zhai, Y., Venter, C., Manning, G., Structural and functional diversity of the microbial kinome (2008) Plos Biol, 5, pp. 467-478
  • Manning, G., Young, S., Miller, T., Zhai, Y., The protist, Monosiga Brevicollis, has a tyrosine kinase signaling network more elaborate and diverse than found in any known metazoan (2008) Proc Nat Acad Sci USA, 105, pp. 964-9679
  • Manning, G., Plowman, G., Hunter, T., Sudarsanam, S., Evolution of protein kinase signaling from yeast to man (2002) Trends Biochem Sci, 27, pp. 514-520
  • Jimenez, C., Cossio, B., Rivard, C., Beri, T., Carpasso, J., Cell division in the unicellular microalga Dunaliella viridis depends on the phosphorylation of extracellular signal-regulated kinases (ERKs) (2007) J Exp Bot, 58, pp. 1001-1011
  • Ray, D., Dutta, S., Banarjee, S., Banerjee, R., Raha, S., Identification, structure, and phylogenetic relationships of a mitogen-activated protein kinase homologue from the parasitic protist Entamoeba histolytica (2005) Gene, 346, pp. 41-50
  • Levin-Salomon, V., Maayan, I., Avrahami-Moyal, L., Marbach, I., Livnah, O., When expressed in yeast, mammalian mitogen-activated protein kinases lose proper regulation and become spontaneously phosphorylated (2009) Biochem J, 417, pp. 331-340
  • Karlsson, M., Mandl, M., Keyse, S.M., Spatio-temporal regulation of mitogen-activated protein kinase (MAPK) signaling by protein phosphatases (2006) Biochem Soc Trans, 34, pp. 842-845
  • Crews, C.M., Alessandrini, A.A., Erikson, R.L., Mouse Erk-1 gene product is a serine/threonine protein kinase that has the potential to phosphorylate tyrosine (1991) Proc Natl Acad Sci USA, 88, pp. 8845-8849
  • Ando, R., Mizuno, H., Miyawaki, A., Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting (2004) Science, 306, pp. 1370-1373
  • Galli S, Labato MI, Bal de Kier Joffe E, Carreras MC, Poderoso JJ (2003) Decreased mitochondrial nitric oxide synthase activity and hydrogen peroxide relate persistent tumoral proliferation to embryonic behaviour. Cancer Res 63: 6370-77; Carreras, M.C., Converso, D., Lorenti, A., Barbich, M., Levisman, D., Mitocondrial nitric oxide synthase drives redox signals for proliferation and quiescence in rat liver development (2004) Hepatology, 40, pp. 157-166
  • Ping, P., Song, C., Zhang, J., Guo, Y., Cao, X., Formation of protein kinase Ce-Lck signaling modules confers cardioprotection (2002) J Clin Invest, 109, pp. 499-507
  • Song, C., Vondriska, T.M., Wang, G.W., Klein, J.B., Cao, X., Molecular conformation dictates signaling module formation: Example of PKCe and Src tyrosine kinase (2002) Am J Physiol, 282, pp. H1166-H1171
  • Jahn, O., Hesse, D., Reinelt, M., Kratzin, H.D., Technical innovations for the automated identification of gel-separated proteins by MALDI-TOF mass spectrometry (2006) Anal Bioanal Chem, 386, pp. 92-103
  • Werner, H.B., Kuhlmann, K., Shen, S., Uecker, M., Schardt, A., Proteolipid protein is required for transport of sirtuin 2 into CNS myelin (2007) J Neurosci, 27, pp. 7717-7730
  • Reumann, S., Babujee, L., Ma, C., Wienkoop, S., Siemsen, T., Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways and defense mechanisms (2007) Plant Cell, 19, pp. 3170-3193
  • Shevchenko, A., Wilm, M., Vorm, O., Mann, M., Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels (1996) Anal Chem, 68, pp. 850-858
  • Komiya, T., Mihara, K., Characterization of the intermediates along the import pathway of the precursor into the matrix (1996) J Biol Chem, 271, pp. 22105-22110
  • Bastiaens, P.I.H., Majoul, I.V., Verveer, P.J., Söling, H.D., Jovin, T.M., Imaging the intracellular trafficking and state of the AB5 quaternary structure of cholera toxin (1996) EMBO J, 15, pp. 4246-4253
  • Zinchuk, V., Zinchuk, O., Okada, T., Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: Pushing pixels to explore biological phenomena (2007) Acta Histochem Cytochem, 40, pp. 101-111
  • Cleveland, W.S., Robust locally weighted regression and smoothing scatterplots (1979) J Am Stat Assoc, 74, pp. 829-836
  • Yang, Y.H., Dudoit, S., Luu, P., Lin, D.M., Peng, V., Normalization for cDNA microarray data: A robust composite method addressing single and multiple slide systematic variation (2002) Nucleic Acids Res, 30, pp. e15
  • Landgrebe, J., Bretz, F., Brunner, E., Efficient design and analysis of two colour factorial microarray experiments (2004) Computational Statistics & Data Analysis, 50, pp. 499-517
  • Bretz, F., Landgrebe, J., Brunner, E., Multiplicity issues in microarray experiments (2005) Methods Inf Med, 44, pp. 431-437

Citas:

---------- APA ----------
Galli, S., Jahn, O., Hitt, R., Hesse, D., Opitz, L., Plessmann, U., Urlaub, H.,..., Jovin, T.M. (2009) . A new paradigm for MAPK: Structural interactions of hERK1 with mitochondria in HeLa cells. PLoS ONE, 4(10).
http://dx.doi.org/10.1371/journal.pone.0007541
---------- CHICAGO ----------
Galli, S., Jahn, O., Hitt, R., Hesse, D., Opitz, L., Plessmann, U., et al. "A new paradigm for MAPK: Structural interactions of hERK1 with mitochondria in HeLa cells" . PLoS ONE 4, no. 10 (2009).
http://dx.doi.org/10.1371/journal.pone.0007541
---------- MLA ----------
Galli, S., Jahn, O., Hitt, R., Hesse, D., Opitz, L., Plessmann, U., et al. "A new paradigm for MAPK: Structural interactions of hERK1 with mitochondria in HeLa cells" . PLoS ONE, vol. 4, no. 10, 2009.
http://dx.doi.org/10.1371/journal.pone.0007541
---------- VANCOUVER ----------
Galli, S., Jahn, O., Hitt, R., Hesse, D., Opitz, L., Plessmann, U., et al. A new paradigm for MAPK: Structural interactions of hERK1 with mitochondria in HeLa cells. PLoS ONE. 2009;4(10).
http://dx.doi.org/10.1371/journal.pone.0007541