Unconventional EGF-induced ERK1/2-mediated Kv1.3 endocytosis
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  • 作者:Ramón Martínez-Mármol ; Núria Comes…
  • 关键词:Olfactory bulb ; Sensory neurons ; Map kinases ; Tyrosine kinases ; Endocytosis ; Voltage ; dependent potassium channels
  • 刊名:Cellular and Molecular Life Sciences (CMLS)
  • 出版年:2016
  • 出版时间:April 2016
  • 年:2016
  • 卷:73
  • 期:7
  • 页码:1515-1528
  • 全文大小:2,592 KB
  • 参考文献:1.Lledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179–193CrossRef PubMed
    2.Menezes JR, Smith CM, Nelson KC, Luskin MB (1995) The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol Cell Neurosci 6:496–508CrossRef PubMed
    3.Lichtenwalner RJ, Parent JM (2006) Adult neurogenesis and the ischemic forebrain. J Cereb Blood Flow Metab 26:1–20CrossRef PubMed
    4.Doetsch F, Petreanu L, Caille I, Garcia-Verdugo JM, Alvarez-Buylla A (2002) EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron 36:1021–1034CrossRef PubMed
    5.Wong RW, Guillaud L (2004) The role of epidermal growth factor and its receptors in mammalian CNS. Cytokine Growth Factor Rev 15:147–156CrossRef PubMed
    6.Sashihara S, Tsuji S, Matsui T (1998) Oncogenes and signal transduction pathways involved in the regulation of Na+ channel expression. Crit Rev Oncog 9:19–34CrossRef PubMed
    7.Hille B (2001) Ion channels of excitable membranes, 3rd edn. Sinauer, Sunderland
    8.Fadool DA, Levitan IB (1998) Modulation of olfactory bulb neuron potassium current by tyrosine phosphorylation. J Neurosci 18:6126–6137PubMed
    9.Doczi MA, Morielli AD, Damon DH (2008) Kv1.3 channels in postganglionic sympathetic neurons: expression, function, and modulation. Am J Physiol Regul Integr Comp Physiol 295:R733–R740CrossRef PubMed PubMedCentral
    10.Fadool DA, Tucker K, Perkins R, Fasciani G, Thompson RN, Parsons AD, Overton JM, Koni PA, Flavell RA, Kaczmarek LK (2004) Kv1.3 channel gene-targeted deletion produces “Super-Smeller Mice” with altered glomeruli, interacting scaffolding proteins, and biophysics. Neuron 41:389–404CrossRef PubMed PubMedCentral
    11.Vicente R, Escalada A, Coma M, Fuster G, Sanchez-Tillo E, Lopez-Iglesias C, Soler C, Solsona C, Celada A, Felipe A (2003) Differential voltage-dependent K+ channel responses during proliferation and activation in macrophages. J Biol Chem 278:46307–46320CrossRef PubMed
    12.Villalonga N, David M, Bielanska J, Gonzalez T, Parra D, Soler C, Comes N, Valenzuela C, Felipe A (2010) Immunomodulatory effects of diclofenac in leukocytes through the targeting of Kv1.3 voltage-dependent potassium channels. Biochem Pharmacol 80:858–866CrossRef PubMed
    13.Bowlby MR, Fadool DA, Holmes TC, Levitan IB (1997) Modulation of the Kv1.3 potassium channel by receptor tyrosine kinases. J Gen Physiol 110:601–610CrossRef PubMed PubMedCentral
    14.Holmes TC, Fadool DA, Levitan IB (1996) Tyrosine phosphorylation of the Kv1.3 potassium channel. J Neurosci 16:1581–1590PubMed
    15.Holmes TC, Fadool DA, Ren R, Levitan IB (1996) Association of Src tyrosine kinase with a human potassium channel mediated by SH3 domain. Science 274:2089–2091CrossRef PubMed
    16.Fadool DA, Tucker K, Phillips JJ, Simmen JA (2000) Brain insulin receptor causes activity-dependent current suppression in the olfactory bulb through multiple phosphorylation of Kv1.3. J Neurophysiol 83:2332–2348PubMed PubMedCentral
    17.Cook KK, Fadool DA (2002) Two adaptor proteins differentially modulate the phosphorylation and biophysics of Kv1.3 ion channel by SRC kinase. J Biol Chem 277:13268–13280CrossRef PubMed PubMedCentral
    18.Colley B, Tucker K, Fadool DA (2004) Comparison of modulation of Kv1.3 channel by two receptor tyrosine kinases in olfactory bulb neurons of rodents. Receptors Channels 10:25–36CrossRef PubMed PubMedCentral
    19.Vicente R, Villalonga N, Calvo M, Escalada A, Solsona C, Soler C, Tamkun MM, Felipe A (2008) Kv1.5 association modifies Kv1.3 traffic and membrane localization. J Biol Chem 283:8756–8764CrossRef PubMed PubMedCentral
    20.Villalonga N, Escalada A, Vicente R, Sanchez-Tillo E, Celada A, Solsona C, Felipe A (2007) Kv1.3/Kv1.5 heteromeric channels compromise pharmacological responses in macrophages. Biochem Biophys Res Commun 352:913–918CrossRef PubMed
    21.Sole L, Roura-Ferrer M, Perez-Verdaguer M, Oliveras A, Calvo M, Fernandez-Fernandez JM, Felipe A (2009) KCNE4 suppresses Kv1.3 currents by modulating trafficking, surface expression and channel gating. J Cell Sci 122:3738–3748CrossRef PubMed
    22.Martinez-Marmol R, Perez-Verdaguer M, Roig SR, Vallejo-Gracia A, Gotsi P, Serrano-Albarras A, Bahamonde MI, Ferrer-Montiel A, Fernandez-Ballester G, Comes N, Felipe A (2013) A non-canonical di-acidic signal at the C-terminus of Kv1.3 determines anterograde trafficking and surface expression. J Cell Sci 126:5681–5691CrossRef PubMed
    23.Shimkets RA, Lifton RP, Canessa CM (1997) The activity of the epithelial sodium channel is regulated by clathrin-mediated endocytosis. J Biol Chem 272:25537–25541CrossRef PubMed
    24.Mankouri J, Taneja TK, Smith AJ, Ponnambalam S, Sivaprasadarao A (2006) Kir6.2 mutations causing neonatal diabetes prevent endocytosis of ATP-sensitive potassium channels. EMBO J 25:4142–4151CrossRef PubMed PubMedCentral
    25.Lukacs GL, Segal G, Kartner N, Grinstein S, Zhang F (1997) Constitutive internalization of cystic fibrosis transmembrane conductance regulator occurs via clathrin-dependent endocytosis and is regulated by protein phosphorylation. Biochem J 328(Pt 2):353–361CrossRef PubMed PubMedCentral
    26.Nesti E, Everill B, Morielli AD (2004) Endocytosis as a mechanism for tyrosine kinase-dependent suppression of a voltage-gated potassium channel. Mol Biol Cell 15:4073–4088CrossRef PubMed PubMedCentral
    27.Fadool DA, Holmes TC, Berman K, Dagan D, Levitan IB (1997) Tyrosine phosphorylation modulates current amplitude and kinetics of a neuronal voltage-gated potassium channel. J Neurophysiol 78:1563–1573PubMed
    28.Gonzalez-Perez O, Quinones-Hinojosa A (2010) Dose-dependent effect of EGF on migration and differentiation of adult subventricular zone astrocytes. Glia 58:975–983PubMed PubMedCentral
    29.Chazal G, Durbec P, Jankovski A, Rougon G, Cremer H (2000) Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J Neurosci 20:1446–1457PubMed
    30.Fontana X, Nacher J, Soriano E, del Rio JA (2006) Cell proliferation in the adult hippocampal formation of rodents and its modulation by entorhinal and fimbria-fornix afferents. Cereb Cortex 16:301–312CrossRef PubMed
    31.Carter RE, Sorkin A (1998) Endocytosis of functional epidermal growth factor receptor-green fluorescent protein chimera. J Biol Chem 273:35000–35007CrossRef PubMed
    32.Fortian A, Sorkin A (2014) Live-cell fluorescence imaging reveals high stoichiometry of Grb2 binding to the EGF receptor sustained during endocytosis. J Cell Sci 127:432–444CrossRef PubMed PubMedCentral
    33.Llado A, Tebar F, Calvo M, Moreto J, Sorkin A, Enrich C (2004) Protein kinaseCdelta-calmodulin crosstalk regulates epidermal growth factor receptor exit from early endosomes. Mol Biol Cell 15:4877–4891CrossRef PubMed PubMedCentral
    34.Sorkina T, Miranda M, Dionne KR, Hoover BR, Zahniser NR, Sorkin A (2006) RNA interference screen reveals an essential role of Nedd4-2 in dopamine transporter ubiquitination and endocytosis. J Neurosci 26:8195–8205CrossRef PubMed
    35.Huang F, Khvorova A, Marshall W, Sorkin A (2004) Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J Biol Chem 279:16657–16661CrossRef PubMed
    36.Sorkina T, Hoover BR, Zahniser NR, Sorkin A (2005) Constitutive and protein kinase C-induced internalization of the dopamine transporter is mediated by a clathrin-dependent mechanism. Traffic 6:157–170CrossRef PubMed
    37.Szilagyi O, Boratko A, Panyi G, Hajdu P (2013) The role of PSD-95 in the rearrangement of Kv1.3 channels to the immunological synapse. Pflugers Arch 465:1341–1353CrossRef PubMed
    38.Galperin E, Abdelmoti L, Sorkin A (2012) Shoc2 is targeted to late endosomes and required for Erk1/2 activation in EGF-stimulated cells. PLoS ONE 7:e36469CrossRef PubMed PubMedCentral
    39.Booth RE, Stockand JD (2003) Targeted degradation of ENaC in response to PKC activation of the ERK1/2 cascade. Am J Physiol Renal Physiol 284:F938–F947CrossRef PubMed
    40.Zeng WZ, Babich V, Ortega B, Quigley R, White SJ, Welling PA, Huang CL (2002) Evidence for endocytosis of ROMK potassium channel via clathrin-coated vesicles. Am J Physiol Renal Physiol 283:F630–F639CrossRef PubMed
    41.Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687–702CrossRef PubMed PubMedCentral
    42.Gonzalez-Perez O, Romero-Rodriguez R, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2009) Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells 27:2032–2043CrossRef PubMed PubMedCentral
    43.Chittajallu R, Chen Y, Wang H, Yuan X, Ghiani CA, Heckman T, McBain CJ, Gallo V (2002) Regulation of Kv1 subunit expression in oligodendrocyte progenitor cells and their role in G1/S phase progression of the cell cycle. Proc Natl Acad Sci U S A 99:2350–2355CrossRef PubMed PubMedCentral
    44.Kues WA, Wunder F (1992) Heterogeneous expression patterns of mammalian potassium channel genes in developing and adult rat brain. Eur J Neurosci 4:1296–1308CrossRef PubMed
    45.Yasuda T, Bartlett PF, Adams DJ (2008) K(ir) and K(v) channels regulate electrical properties and proliferation of adult neural precursor cells. Mol Cell Neurosci 37:284–297CrossRef PubMed
    46.Liebau S, Propper C, Bockers T, Lehmann-Horn F, Storch A, Grissmer S, Wittekindt OH (2006) Selective blockage of Kv1.3 and Kv3.1 channels increases neural progenitor cell proliferation. J Neurochem 99:426–437CrossRef PubMed
    47.Tegla CA, Cudrici C, Rozycka M, Soloviova K, Ito T, Singh AK, Khan A, Azimzadeh P, Andrian-Albescu M, Niculescu F, Rus V, Judge SI, Rus H (2011) C5b-9-activated, K(v)1.3 channels mediate oligodendrocyte cell cycle activation and dedifferentiation. Exp Mol Pathol 91:335–345CrossRef PubMed PubMedCentral
    48.Wang T, Lee MH, Johnson T, Allie R, Hu L, Calabresi PA, Nath A (2010) Activated T-cells inhibit neurogenesis by releasing granzyme B: rescue by Kv1.3 blockers. J Neurosci 30:5020–5027CrossRef PubMed PubMedCentral
    49.Marks DR, Fadool DA (2007) Post-synaptic density perturbs insulin-induced Kv1.3 channel modulation via a clustering mechanism involving the SH3 domain. J Neurochem 103:1608–1627CrossRef PubMed PubMedCentral
    50.Rus H, Pardo CA, Hu L, Darrah E, Cudrici C, Niculescu T, Niculescu F, Mullen KM, Allie R, Guo L, Wulff H, Beeton C, Judge SI, Kerr DA, Knaus HG, Chandy KG, Calabresi PA (2005) The voltage-gated potassium channel Kv1.3 is highly expressed on inflammatory infiltrates in multiple sclerosis brain. Proc Natl Acad Sci U S A 102:11094–11099CrossRef PubMed PubMedCentral
    51.Varga Z, Csepany T, Papp F, Fabian A, Gogolak P, Toth A, Panyi G (2009) Potassium channel expression in human CD4+ regulatory and naive T cells from healthy subjects and multiple sclerosis patients. Immunol Lett 124:95–101CrossRef PubMed
    52.Scalabrino G, Tredici G, Buccellato FR, Manfridi A (2000) Further evidence for the involvement of epidermal growth factor in the signaling pathway of vitamin B12 (cobalamin) in the rat central nervous system. J Neuropathol Exp Neurol 59:808–814CrossRef PubMed
    53.Vennekamp J, Wulff H, Beeton C, Calabresi PA, Grissmer S, Hansel W, Chandy KG (2004) Kv1.3-blocking 5-phenylalkoxypsoralens: a new class of immunomodulators. Mol Pharmacol 65:1364–1374CrossRef PubMed
    54.Norton RS, Pennington MW, Wulff H (2004) Potassium channel blockade by the sea anemone toxin ShK for the treatment of multiple sclerosis and other autoimmune diseases. Curr Med Chem 11:3041–3052CrossRef PubMed
  • 作者单位:Ramón Martínez-Mármol (1) (2)
    Núria Comes (1)
    Katarzyna Styrczewska (1)
    Mireia Pérez-Verdaguer (1)
    Rubén Vicente (3)
    Lluís Pujadas (2)
    Eduardo Soriano (2) (4) (5)
    Alexander Sorkin (6)
    Antonio Felipe (1) (7)

    1. Molecular Physiology Laboratory, Departament de Bioquímica i Biologia Molecular, Institut de Biomedicina (IBUB), Barcelona, Spain
    2. Departament de Biologia Celular, Universitat de Barcelona, Barcelona, Spain
    3. Laboratory of Molecular Physiology and Channelopathies, Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, Barcelona, Spain
    4. Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), ISCIII, Madrid, Spain
    5. Vall d´Hebron Institute of Research (VHIR) and Institució Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Spain
    6. Department of Cell Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
    7. Departament de Bioquímica i Biologia Molecular, Universitat de Barcelona, Avda. Diagonal 643, 08028, Barcelona, Spain
  • 刊物类别:Biomedical and Life Sciences
  • 刊物主题:Life Sciences
    Cell Biology
    Biomedicine
    Life Sciences
    Biochemistry
  • 出版者:Birkh盲user Basel
  • ISSN:1420-9071
文摘
The potassium channel Kv1.3 plays roles in immunity, neuronal development and sensory discrimination. Regulation of Kv1.3 by kinase signaling has been studied. In this context, EGF binds to specific receptors (EGFR) and triggers tyrosine kinase-dependent signaling, which down-regulates Kv1.3 currents. We show that Kv1.3 undergoes EGF-dependent endocytosis. This EGF-mediated mechanism is relevant because is involved in adult neural stem cell fate determination. We demonstrated that changes in Kv1.3 subcellular distribution upon EGFR activation were due to Kv1.3 clathrin-dependent endocytosis, which targets the Kv1.3 channels to the lysosomal degradative pathway. Interestingly, our results further revealed that relevant tyrosines and other interacting motifs, such as PDZ and SH3 domains, were not involved in the EGF-dependent Kv1.3 internalization. However, a new, and yet undescribed mechanism, of ERK1/2-mediated threonine phosphorylation is crucial for the EGF-mediated Kv1.3 endocytosis. Our results demonstrate that EGF triggers the down-regulation of Kv1.3 activity and its expression at the cell surface, which is important for the development and migration of adult neural progenitors.

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