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Abstract:

CRH is a key regulator of neuroendocrine, autonomic, and behavioral response to stress. CRHstimulated CRH receptor 1 (CRHR1) activates ERK1/2 depending on intracellular context. In a previous work, we demonstrated that CRH activates ERK1/2 in limbic areas of the mouse brain (hippocampus and basolateral amygdala). ERK1/2 is an essential mediator of hippocampal physiological processes including emotional behavior, synaptic plasticity, learning, and memory. To elucidate the molecular mechanisms by which CRH activates ERK1/2 in hippocampal neurons, we used the mouse hippocampal cell line HT22. We document for the first time that ERK1/2 activation in response to CRH is biphasic, involving a first cAMP- and B-Raf-dependent early phase and a second phase that critically depends on CRHR1 internalization and β-arrestin2. By means of mass-spectrometry-based screening, we identified B-Raf-associated proteins that coimmunoprecipitate with endogenous B-Raf after CRHR1 activation. Using molecular and pharmacological tools, the functional impact of selected B-Raf partners in CRH-dependent ERK1/2 activation was dissected. These results indicate that 14-3-3 proteins, protein kinase A, and Rap1, are essential for early CRH-induced ERK1/2 activation, whereas dynamin and vimentin are required for the CRHR1 internalization-dependent phase. Both phases of ERK1/2 activation depend on calcium influx and are affected by calcium/calmodulin-dependent protein kinase II inactivation. Thus, this report describes the dynamics and biphasic nature of ERK1/2 activation downstream neuronal CRHR1 and identifies several new critical components of the CRHR1 signaling machinery that selectively controls the early and late phases of ERK1/2 activation, thus providing new potential therapeutic targets for stress-related disorders. © 2013 by The Endocrine Society.

Registro:

Documento: Artículo
Título:B-Raf and CRHR1 internalization mediate biphasic ERK1/2 activation by CRH in hippocampal HT22 cells
Autor:Bonfiglio, J.J.; Inda, C.; Senin, S.; Maccarrone, G.; Refojo, D.; Giacomini, D.; Turck, C.W.; Holsboer, F.; Arzt, E.; Silberstein, S.
Filiación:Instituto de Investigación en Biomedicina de Buenos Aires, Consejo Nacional de Investigaciones Científicas y Técnicas, Partner Institute of the Max Planck Society, Godoy Cruz 2390, C1425FQA, Buenos Aires, Argentina
Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 1428 Buenos Aires, Argentina
Max Planck Institute of Psychiatry, 80804 Munich, Germany
Palabras clave:B Raf kinase; beta arrestin 2; calcium; calcium calmodulin dependent protein kinase II; corticotropin releasing factor; corticotropin releasing factor receptor 1; cyclic AMP; cyclic AMP dependent protein kinase; dynamin; mitogen activated protein kinase 1; protein 14 3 3; Rap1 protein; vimentin; animal cell; article; basolateral amygdala; behavior; calcium cell level; calcium transport; cellular distribution; controlled study; enzyme activation; enzyme inactivation; hippocampus; internalization; learning; mass spectrometry; memory; mouse; nerve cell plasticity; nonhuman; physiological process; priority journal; screening; Adenylate Cyclase; Animals; Arrestins; Calcium; Calcium-Calmodulin-Dependent Protein Kinase Type 2; Corticotropin-Releasing Hormone; Cyclic AMP; Endocytosis; Enzyme Activation; Hippocampus; Humans; Mice; Mitogen-Activated Protein Kinase 1; Mitogen-Activated Protein Kinase 3; Models, Biological; Proto-Oncogene Proteins B-raf; Rats; Receptors, Corticotropin-Releasing Hormone; Signal Transduction; Subcellular Fractions; Time Factors; Vimentin
Año:2013
Volumen:27
Número:3
Página de inicio:491
Página de fin:510
DOI: http://dx.doi.org/10.1210/me.2012-1359
Título revista:Molecular Endocrinology
Título revista abreviado:Mol. Endocrinol.
ISSN:08888809
CODEN:MOENE
CAS:calcium, 14092-94-5, 7440-70-2; calcium calmodulin dependent protein kinase II, 141467-21-2; corticotropin releasing factor, 178359-01-8, 79804-71-0, 86297-72-5, 86784-80-7, 9015-71-8; cyclic AMP, 60-92-4; mitogen activated protein kinase 1, 137632-08-7; protein 14 3 3, 136047-16-0; Adenylate Cyclase, 4.6.1.1; Arrestins; CRF receptor type 1; Calcium, 7440-70-2; Calcium-Calmodulin-Dependent Protein Kinase Type 2, 2.7.11.17; Corticotropin-Releasing Hormone, 9015-71-8; Cyclic AMP, 60-92-4; Mitogen-Activated Protein Kinase 1, 2.7.11.24; Mitogen-Activated Protein Kinase 3, 2.7.11.24; Proto-Oncogene Proteins B-raf, 2.7.11.1; Receptors, Corticotropin-Releasing Hormone; Vimentin; beta-arrestin
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Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_08888809_v27_n3_p491_Bonfiglio

Referencias:

  • Vale, W., Spiess, J., Rivier, C., Rivier, J., Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin (1981) Science, 213, pp. 1394-1397
  • de Kloet, E.R., Joels, M., Holsboer, F., Stress and the brain: From adaptation to disease (2005) Nat Rev Neurosci, 6, pp. 463-475
  • Smith, S.M., Vale, W.W., The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress (2006) Dialogues Clin Neurosci, 8, pp. 383-395
  • Gallagher, J.P., Orozco-Cabal, L.F., Liu, J., Shinnick-Gallagher, P., Synaptic physiology of central CRH system (2008) Eur J Pharmacol, 583, pp. 215-225
  • Arborelius, L., Owens, M.J., Plotsky, P.M., Nemeroff, C.B., The role of corticotropin-releasing factor in depression and anxiety disorders (1999) J Endocrinol, 160, pp. 1-12
  • Holsboer, F., The rationale for corticotropin-releasing hormone receptor (CRH-R) antagonists to treat depression and anxiety (1999) J Psychiatr Res, 33, pp. 181-214
  • Holsboer, F., Ising, M., Stress hormone regulation: Biological role and translation into therapy (2010) Annu Rev Psychol, 61, pp. 81-109+9C1-C11
  • Grigoriadis, D.E., The corticotropin-releasing factor receptor: A novel target for the treatment of depression and anxiety-related disorders (2005) Expert Opin Ther Targets, 9, pp. 651-684
  • Holsboer, F., Ising, M., Central CRH system in depression and anxiety: Evidence from clinical studies with CRH1 receptor antagonists (2008) Eur J Pharmacol, 583, pp. 350-357
  • Smith, G.W., Aubry, J.M., Dellu, F., Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development (1998) Neuron, 20, pp. 1093-1102
  • Muller, M.B., Zimmermann, S., Sillaber, I., Limbic corticotropin-releasing hormone receptor 1 mediates anxiety-related behavior and hormonal adaptation to stress (2003) Nat Neurosci, 6, pp. 1100-1107
  • Refojo, D., Echenique, C., Muller, M.B., Corticotropin-releasing hormone activates ERK1/2 MAPK in specific brain areas (2005) Proc Natl Acad Sci U S A, 102, pp. 6183-6188
  • Wang, X.D., Chen, Y., Wolf, M., Forebrain CRHR1 deficiency attenuates chronic stress-induced cognitive deficits and dendritic remodeling (2011) Neurobiol Dis, 42, pp. 300-310
  • Refojo, D., Schweizer, M., Kuehne, C., Glutamatergic and dopaminergic neurons mediate anxiogenic and anxiolytic effects of CRHR1 (2011) Science, 333, pp. 1903-1907
  • Bonfiglio, J.J., Inda, C., Refojo, D., Holsboer, F., Arzt, E., Silberstein, S., The corticotropin-releasing hormone network and the hypothalamic-pitu-itary-adrenal axis: Molecularandcellular mechanisms involved (2011) Neuroendocrinology, 94, pp. 12-20
  • Hillhouse, E.W., Grammatopoulos, D.K., The molecular mechanisms underlying the regulation of the biological activity of corticotropinreleasing hormone receptors: Implications for physiology and pathophysiology (2006) Endocr Rev, 27, pp. 260-286
  • Dautzenberg, F.M., Hauger, R.L., The CRF peptide family and their receptors: Yet more partners discovered (2002) Trends Pharmacol Sci, 23, pp. 71-77
  • Punn, A., Levine, M.A., Grammatopoulos, D.K., Identification of signaling molecules mediating corticotropin-releasing hormone-R1α-mitogen-activated protein kinase (MAPK) interactions: The critical role of phosphatidylinositol 3-kinase in regulating ERK1/2 but not p38 MAPK activation (2006) Mol Endocrinol, 20, pp. 3179-3195
  • Arzt, E., Holsboer, F., CRF signaling: Molecular specificity for drug targeting in the CNS (2006) Trends Pharmacol Sci, 27, pp. 531-538
  • Teli, T., Markovic, D., Hewitt, M.E., Levine, M.A., Hillhouse, E.W., Grammatopoulos, D.K., Structural domains determining signalling characteristics of the CRH-receptor type 1 variant R1β and response to PKC phosphorylation (2008) Cell Signal, 20, pp. 40-49
  • Grammatopoulos, D.K., Randeva, H.S., Levine, M.A., Katsanou, E.S., Hillhouse, E.W., Urocortin, but not corticotropin-releasing hormone (CRH), activates the mitogen-activated protein kinase signal transduction pathway in human pregnant myometrium: An effect mediated via R1α and R2β CRH receptor subtypes and stimulation of Gq-proteins (2000) Mol Endocrinol, 14, pp. 2076-2091
  • Cao, J., Cetrulo, C.L., Theoharides, T.C., Corticotropin-releasing hormone induces vascular endothelial growth factor release from human mast cells via the cAMP/protein kinase A/p38 mitogen-activated protein kinase pathway (2006) Mol Pharmacol, 69, pp. 998-1006
  • Cibelli, G., Corsi, P., Diana, G., Vitiello, F., Thiel, G., Corticotropinreleasing factor triggers neurite outgrowth of a catecholaminergic immortalized neuron via cAMP and MAP kinase signalling pathways (2001) Eur J Neurosci, 13, pp. 1339-1348
  • Kovalovsky, D., Refojo, D., Liberman, A.C., Activation and induction of NUR77/NURR1 in corticotrophs by CRH/cAMP: Involvement of calcium, protein kinase A, and MAPK pathways (2002) Mol Endocrinol, 16, pp. 1638-1651
  • van Kolen, K., Dautzenberg, F.M., Verstraeten, K., Corticotropin releasing factor-induced ERK phosphorylation in AtT20 cells occurs via a cAMP-dependent mechanism requiring EPAC2 (2010) Neuropharmacology, 58, pp. 135-144
  • Huising, M.O., van der Meulen, T., Vaughan, J.M., CRFR1 is expressed on pancreatic beta cells, promotes beta cell proliferation, and potentiates insulin secretion in a glucose-dependent manner (2010) Proc Natl Acad Sci U S A, 107, pp. 912-917
  • Dautzenberg, F.M., Gutknecht, E., van der Linden, I., Olivares-Reyes, J.A., Durrenberger, F., Hauger, R.L., Cell-type specific calcium signaling by corticotropin-releasing factor type 1 (CRF1) and 2a (CRF2(a) receptors: Phospholipase C-mediated responses in human embryonic kidney 293 but not SK-N-MC neuroblastoma cells (2004) Biochem Pharmacol., 68, pp. 1833-1844
  • Gutknecht, E., van der Linden, I., van Kolen, K., Verhoeven, K.F., Vauquelin, G., Dautzenberg, F.M., Molecular mechanisms of corticotropin-releasing factor receptor-induced calcium signaling (2009) Mol Pharmacol, 75, pp. 648-657
  • Wu, S.V., Yuan, P.Q., Lai, J., Activation of Type 1 CRH receptor isoforms induces serotonin release from human carcinoid BON-1N cells: An enterochromaffin cell model (2011) Endocrinology, 152, pp. 126-137
  • Ortiz, J., Harris, H.W., Guitart, X., Terwilliger, R.Z., Haycock, J.W., Nestler, E.J., Extracellular signal-regulated protein kinases (ERKs) and ERK kinase (MEK) in brain: Regional distribution and regulation by chronic morphine (1995) J Neurosci, 15, pp. 1285-1297
  • Di Benedetto, B., Hitz, C., Holter, S.M., Kuhn, R., Vogt Weisenhorn, D.M., Wurst, W., Differential mRNA distribution of components of the ERK/MAPK signalling cascade in the adult mouse brain (2007) J Comp Neurol, 500, pp. 542-556
  • Thomas, G.M., Huganir, R.L., MAPK cascade signalling and synaptic plasticity (2004) Nat Rev Neurosci, 5, pp. 173-183
  • Samuels, I.S., Saitta, S.C., Landreth, G.E., MAP'ing CNS development and cognition: An ERKsome process (2009) Neuron, 61, pp. 160-167
  • Davis, S., Laroche, S., Mitogen-activated protein kinase/extracellular regulated kinase signalling and memory stabilization: A review (2006) Genes Brain Behav, 5 (SUPPL. 2), pp. 61-72
  • Meller, E., Shen, C., Nikolao, T.A., Region-specific effects of acute and repeated restraint stress on the phosphorylation of mitogenactivated protein kinases (2003) Brain Res, 979, pp. 57-64
  • Qi, X., Lin, W., Li, J., Pan, Y., Wang, W., The depressive-like behaviors are correlated with decreased phosphorylation of mitogen-activated protein kinases in rat brain following chronic forced swim stress (2006) Behav Brain Res, 175, pp. 233-240
  • Einat, H., Yuan, P., Gould, T.D., The role of the extracellular signal-regulated kinase signaling pathway in mood modulation (2003) J Neurosci, 23, pp. 7311-7316
  • Ailing, F., Fan, L., Li, S., Manji, S., Role of extracellular signal-regulated kinase signal transduction pathway in anxiety (2008) J Psychiatr Res, 43, pp. 55-63
  • Todorovic, C., Sherrin, T., Pitts, M., Hippel, C., Rayner, M., Spiess, J., Suppression of the MEK/ERK signaling pathway reverses depression-like behaviors of CRF2-deficient mice (2009) Neuropsychopharmacology, 34, pp. 1416-1426
  • Liu, J., Li, L., Suo, W.Z., HT22 hippocampal neuronal cell line possesses functional cholinergic properties (2009) Life Sci, 84, pp. 267-271
  • Aminova, L.R., Chavez, J.C., Lee, J., Prosurvival and prodeath effects of hypoxia-inducible factor-1α stabilization in a murine hippocampal cell line (2005) J Biol Chem, 280, pp. 3996-4003
  • Stanciu, M., Wang, Y., Kentor, R., Persistent activation of ERK contributes to glutamate-induced oxidative toxicity in a neuronal cell line and primary cortical neuron cultures (2000) J Biol Chem, 275, pp. 12200-12206
  • Davis, J.B., Maher, P., Protein kinase C activation inhibits glutamateinduced cytotoxicity in a neuronal cell line (1994) Brain Res, 652, pp. 169-173
  • Caldwell, J.D., Shapiro, R.A., Jirikowski, G.F., Suleman, F., Internalization of sex hormone-binding globulin into neurons and brain cells in vitro and in vivo (2007) Neuroendocrinology, 86, pp. 84-93
  • Li, Y., Maher, P., Schubert, D., A role for 12-lipoxygenase in nerve cell death caused by glutathione depletion (1997) Neuron, 19, pp. 453-463
  • Luo, Y., DeFranco, D.B., Opposing roles for ERK1/2 in neuronal oxidative toxicity: Distinct mechanisms of ERK1/2 action at early versus late phases of oxidative stress (2006) J Biol Chem, 281, pp. 16436-16442
  • van Leyen, K., Siddiq, A., Ratan, R.R., Lo, E.H., Proteasome inhibition protects HT22 neuronal cells from oxidative glutamate toxicity (2005) J Neurochem, 92, pp. 824-830
  • Tobaben, S., Grohm, J., Seiler, A., Conrad, M., Plesnila, N., Culmsee, C., Bid-mediated mitochondrial damage is a key mechanism in glutamate-induced oxidative stress and AIF-dependent cell death in immortalized HT-22 hippocampal neurons (2011) Cell Death Differ, 18, pp. 282-292
  • Bonfiglio, J.J., McCarrone, G., Rewerts, C., Characterization of the B-Raf interactome in mouse hippocampal neuronal cells (2011) J Proteomics, 74, pp. 186-198
  • Perkins, D.N., Pappin, D.J., Creasy, D.M., Cottrell, J.S., Probability-based protein identification by searching sequence databases using mass spectrometry data (1999) Electrophoresis, 20, pp. 3551-3567
  • Davio, C.A., Cricco, G.P., Bergoc, R.M., Rivera, E.S., H1 and H2 histamine receptors in N-nitroso-N-methylurea (NMU)-induced carcinomas with atypical coupling to signal transducers (1995) Biochem Pharmacol, 50, pp. 91-96
  • Holmes, K.D., Babwah, A.V., Dale, L.B., Poulter, M.O., Ferguson, S.S., Differential regulation of corticotropin releasing factor 1α receptor endocytosis and trafficking by β-arrestins and Rab GTPases (2006) J Neurochem, 96, pp. 934-949
  • Vossler, M.R., Yao, H., York, R.D., Pan, M.G., Rim, C.S., Stork, P.J., cAMP activates MAP kinase and Elk-1 through a B-Raf-and Rap1-dependent pathway (1997) Cell, 89, pp. 73-82
  • Ritt, D.A., Zhou, M., Conrads, T.P., Veenstra, T.D., Copeland, T.D., Morrison, D.K., CK2 Is a component of the KSR1 scaffold complex that contributes to Raf kinase activation (2007) Curr Biol, 17, pp. 179-184
  • Brummer, T., Martin, P., Herzog, S., Misawa, Y., Daly, R.J., Reth, M., Functional analysis of the regulatory requirements of B-Raf and the B-Raf(V600E) oncoprotein (2006) Oncogene, 25, pp. 6262-6276
  • Tzivion, G., Luo, Z., Avruch, J., A dimeric 14-3-3 protein is an essential cofactor for Raf kinase activity (1998) Nature, 394, pp. 88-92
  • Fischer, A., Baljuls, A., Reinders, J., Regulation of RAF activity by 14-3-3 proteins: RAF kinases associate functionally with both homo-and heterodimeric forms of 14-3-3 proteins (2009) J Biol Chem, 284, pp. 3183-3194
  • Thorson, J.A., Yu, L.W., Hsu, A.L., 14-3-3 proteins are required for maintenance of Raf-1 phosphorylation and kinase activity (1998) Mol Cell Biol, 18, pp. 5229-5238
  • Grewal, S.S., Horgan, A.M., York, R.D., Withers, G.S., Banker, G.A., Stork, P.J., Neuronal calcium activates a Rap1 and B-Raf signaling pathway via the cyclic adenosine monophosphate-dependent protein kinase (2000) J Biol Chem, 275, pp. 3722-3728
  • Stork, P.J., Does Rap1 deserve a bad Rap? (2003) Trends Biochem Sci, 28, pp. 267-275
  • McKay, M.M., Ritt, D.A., Morrison, D.K., Signaling dynamics of the KSR1 scaffold complex (2009) Proc Natl Acad Sci U S A, 106, pp. 11022-11027
  • Pierce, K.L., Maudsley, S., Daaka, Y., Luttrell, L.M., Lefkowitz, R.J., Role of endocytosis in the activation of the extracellular signal-regulated kinase cascade by sequestering and nonsequestering G protein-coupled receptors (2000) Proc Natl Acad Sci U S A, 97, pp. 1489-1494
  • Lefkowitz, R.J., Shenoy, S.K., Transduction of receptor signals by β-arrestins (2005) Science, 308, pp. 512-517
  • Luini, A., Lewis, D., Guild, S., Corda, D., Axelrod, J., Hormone secretagogues increase cytosolic calcium by increasing cAMP in corticotropin-secreting cells (1985) Proc Natl Acad Sci U S A, 82, pp. 8034-8038
  • Lee, A.K., Tse, A., Mechanism underlying corticotropin-releasing hormone (CRH) triggered cytosolic Ca2+ rise in identified rat corticotrophs (1997) J Physiol., 504 (PART 2), pp. 367-378
  • Lancaster, B., Hu, H., Gibb, B., Storm, J.F., Kinetics of ion channel modulation by cAMP in rat hippocampal neurones (2006) J Physiol, 576, pp. 403-417
  • Means, A.R., Regulatory cascades involving calmodulin-dependent protein kinases (2000) Mol Endocrinol, 14, pp. 4-13
  • Punn, A., Chen, J., Delidaki, M., Mapping structural determinants within third intracellular loop that direct signaling specificity of type 1 corticotropin-releasing hormone receptor (2012) J Biol Chem, 287, pp. 8974-8985
  • Murphy, L.O., Smith, S., Chen, R.H., Fingar, D.C., Blenis, J., Molecular interpretation of ERK signal duration by immediate early gene products (2002) Nat Cell Biol, 4, pp. 556-564
  • Asimaki, O., Mangoura, D., Cannabinoid receptor 1 induces a biphasic ERK activation via multiprotein signaling complex formation of proximal kinases PKCIe{cyrillic, ukrainian}, Src, and Fyn in primary neurons (2011) Neurochem Int, 58, pp. 135-144
  • Ahn, S., Shenoy, S.K., Wei, H., Lefkowitz, R.J., Differential kinetic and spatial patterns of β-arrestin and G protein-mediated ERK activation by the angiotensin II receptor (2004) J Biol Chem, 279, pp. 35518-35525
  • Silberstein, S., Vogl, A.M., Refojo, D., Amygdaloid pERK1/2 in corticotropin-releasing hormone overexpressing mice under basal and acute stress conditions (2009) Neuroscience, 159, pp. 610-617
  • Bangasser, D.A., Curtis, A., Reyes, B.A., Sex differences in corticotropin-releasing factor receptor signaling and trafficking: Potential role in female vulnerability to stress-related psychopathology (2010) Mol Psychiatry, 15, pp. 877+896-877+904
  • Waselus, M., Nazzaro, C., Valentino, R.J., van Bockstaele, E.J., Stress-induced redistribution of corticotropin-releasing factor receptor subtypes in the dorsal raphe nucleus (2009) Biol Psychiatry, 66, pp. 76-83
  • Song, X., Coffa, S., Fu, H., Gurevich, V.V., How does arrestin assemble MAPKs into a signaling complex? (2009) J Biol Chem, 284, pp. 685-695
  • Luttrell, L.M., Roudabush, F.L., Choy, E.W., Activation and targeting of extracellular signal-regulated kinases by beta-arrestin scaffolds (2001) Proc Natl Acad Sci U S A, 98, pp. 2449-2454
  • Wimmer, R., Baccarini, M., Partner exchange: Protein-protein interactions in the Raf pathway (2010) Trends Biochem Sci, 35, pp. 660-668
  • Rushworth, L.K., Hindley, A.D., O'Neill, E., Kolch, W., Regulation and role of Raf-1/B-Raf heterodimerization (2006) Mol Cell Biol, 26, pp. 2262-2272
  • Galabova-Kovacs, G., Catalanotti, F., Matzen, D., Essential role of B-Raf in oligodendrocyte maturation and myelination during postnatal central nervous system development (2008) J Cell Biol, 180, pp. 947-955
  • Valluet, A., Druillennec, S., Barbotin, C., B-raf and C-raf are required for melanocyte stem cell self-maintenance (2012) Cell Rep, 2, pp. 774-780
  • MacNicol, M.C., Muslin, A.J., McNicol, A.M., Disruption of the 14-3-3 binding site within the B-Raf kinase domain uncouples catalytic activity from PC12 cell differentiation (2000) J Biol Chem, 275, pp. 3803-3809
  • Stork, P.J., Schmitt, J.M., Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation (2002) Trends Cell Biol, 12, pp. 258-266
  • Obara, Y., Horgan, A.M., Stork, P.J., The requirement of Ras and Rap1 for the activation of ERKs by cAMP, PACAP, and KCl in cerebellar granule cells (2007) J Neurochem, 101, pp. 470-482
  • Morozov, A., Muzzio, I.A., Bourtchouladze, R., Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory (2003) Neuron, 39, pp. 309-325
  • Perlson, E., Michaelevski, I., Kowalsman, N., Vimentin binding to phosphorylated Erk sterically hinders enzymatic dephosphorylation of the kinase (2006) J Mol Biol, 364, pp. 938-944
  • Janosch, P., Kieser, A., Eulitz, M., The Raf-1 kinase associates with vimentin kinases and regulates the structure of vimentin filaments (2000) FASEB J, 14, pp. 2008-2021
  • Vallee, R.B., Okamoto, P.M., The regulation of endocytosis: Identifying dynamin's binding partners (1995) Trends Cell Biol, 5, pp. 43-47
  • Xiao, K., McClatchy, D.B., Shukla, A.K., Functional specialization of β-arrestin interactions revealed by proteomic analysis (2007) Proc Natl Acad Sci U S A, 104, pp. 12011-12016
  • DeWire, S.M., Ahn, S., Lefkowitz, R.J., Shenoy, S.K., β-Arrestins and cell signaling (2007) Annu Rev Physiol, 69, pp. 483-510
  • Illario, M., Cavallo, A.L., Bayer, K.U., Calcium/calmodulin-dependent protein kinase II binds to Raf-1 and modulates integrin-stimulated ERK activation (2003) J Biol Chem, 278, pp. 45101-45108
  • Cipolletta, E., Monaco, S., Maione, A.S., Vitiello, L., Campiglia, P., Pastore, L., Franchini, C., Illario, M., Calmodulindependent kinase II mediates vascular smooth muscle cell proliferation and is potentiated by extracellular signal regulated kinase (2010) Endocrinology, 151, pp. 2747-2759
  • Mangmool, S., Shukla, A.K., Rockman, H.A., β-Arrestin-dependent activation of Ca2+ calmodulin kinase II after β1-adrenergic receptor stimulation (2010) J Cell Biol, 189, pp. 573-587
  • Labasque, M., Reiter, E., Becamel, C., Bockaert, J., Marin, P., Physical interaction of calmodulin with the 5-hydroxytryptamine2C receptor C terminus is essential for G protein-independent, arrestin-dependent receptor signaling (2008) Mol Biol Cell, 19, pp. 4640-4650

Citas:

---------- APA ----------
Bonfiglio, J.J., Inda, C., Senin, S., Maccarrone, G., Refojo, D., Giacomini, D., Turck, C.W.,..., Silberstein, S. (2013) . B-Raf and CRHR1 internalization mediate biphasic ERK1/2 activation by CRH in hippocampal HT22 cells. Molecular Endocrinology, 27(3), 491-510.
http://dx.doi.org/10.1210/me.2012-1359
---------- CHICAGO ----------
Bonfiglio, J.J., Inda, C., Senin, S., Maccarrone, G., Refojo, D., Giacomini, D., et al. "B-Raf and CRHR1 internalization mediate biphasic ERK1/2 activation by CRH in hippocampal HT22 cells" . Molecular Endocrinology 27, no. 3 (2013) : 491-510.
http://dx.doi.org/10.1210/me.2012-1359
---------- MLA ----------
Bonfiglio, J.J., Inda, C., Senin, S., Maccarrone, G., Refojo, D., Giacomini, D., et al. "B-Raf and CRHR1 internalization mediate biphasic ERK1/2 activation by CRH in hippocampal HT22 cells" . Molecular Endocrinology, vol. 27, no. 3, 2013, pp. 491-510.
http://dx.doi.org/10.1210/me.2012-1359
---------- VANCOUVER ----------
Bonfiglio, J.J., Inda, C., Senin, S., Maccarrone, G., Refojo, D., Giacomini, D., et al. B-Raf and CRHR1 internalization mediate biphasic ERK1/2 activation by CRH in hippocampal HT22 cells. Mol. Endocrinol. 2013;27(3):491-510.
http://dx.doi.org/10.1210/me.2012-1359