Startseite Lebenswissenschaften Functions of the neuron-specific protein ADAP1 (centaurin-α1) in neuronal differentiation and neurodegenerative diseases, with an overview of structural and biochemical properties of ADAP1
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Functions of the neuron-specific protein ADAP1 (centaurin-α1) in neuronal differentiation and neurodegenerative diseases, with an overview of structural and biochemical properties of ADAP1

  • Rolf Stricker

    Rolf Stricker studied Biochemistry at the University of Tübingen, and graduated in 1992. In 1996 he received his PhD in Biochemistry at the Institute of Physiological Chemistry of the University of Tübingen. From 1994 to March 2014 he worked at the Institute of Neurobiochemistry of the Otto-von-Guericke University, Magdeburg as postdoctoral fellow. Since April 2014 he is a member of the Institute for Biochemistry and Cell Biology of the Otto-von-Guericke University, Magdeburg.

    und Georg Reiser

    Georg Reiser did his PhD at the Max-Planck Institute of Biochemistry in Martinsried and the Ludwig-Maximilians University in Munich under the supervision of B. Hamprecht in the department of F. Lynen. After working as research fellow in the Institute for Physiological Chemistry in Wurzburg, he obtained a DFG-fellowship with further training in electrophysiology at the University College London, Department of Biophysics under R. Miledi. There, he studied nicotinic acetylcholine receptor ion channels. From 1984 he continued research in mechanisms of neural molecular signaling, focusing on calcium regulation and identification of the inositol(1,3,4,5)P4 receptor protein, designated p42IP4. From 1994 he is professor for biochemistry and neurochemistry in Magdeburg, Medical Faculty with research on molecular mechanisms of neuroprotection in ischemia and stroke, covering functions of mitochondria, protease-activated receptors, P2Y nucleotide receptors, nuclear Peroxisome Proliferators Activated Receptors, and iPLA2 isoforms in neurodegenerative diseases.

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Veröffentlicht/Copyright: 23. April 2014

Abstract

Eukaryotic cells express numerous ArfGAPs (ADP-ribosylation factor GTPase-activating proteins). There is increasing knowledge about the function of the brain-specific protein ADAP1 [ArfGAP with dual pleckstrin homology (PH) domain] as well as about its biochemical properties. The ADAP subfamily, also designated centaurin-α, has an N-terminal ArfGAP domain followed by two PH domains. The mammalian ADAP subfamily consists of two identified isoforms, ADAP1 and ADAP2 (centaurin-α1 and -α2). ADAP1 is highly expressed in neurons. We highlight the functional roles of ADAP1 in neuronal differentiation and neurodegeneration. Because of interactions with different proteins and phosphoinositol-lipids, ADAP1 can function as a scaffolding protein in several signal transduction pathways. Firstly, ADAP1 mediates cytoskeletal crosstalk. This is indicated by multiple interactions of ADAP1 with components of the actin and microtubule cytoskeleton. Secondly, regulation of neuronal polarity formation and axon specification by ADAP1 is suggested by crystal structural data obtained for human ADAP1, and the complexes of ADAP1-Ins(1,3,4,5)P4 and/or the forkhead-associated domain of the kinesin KIF13B. These structures support the concept that a KIF13B-ADAP1 complex enhances the local accumulation of PtdIns(3,4,5)P3 at the tips of neurites, and thus favors neuronal polarity. Thirdly, recent evidence unravels a pathological role of ADAP1 because upregulation of ADAP1 by amyloid β-peptide causes ADAP1-Ras-ERK-dependent translocation of Elk-1 to mitochondria. This impairs mitochondrial functions with subsequent synaptic dysfunction and exacerbates neurodegeneration, as in Alzheimer’s disease.


Corresponding author: Georg Reiser, Institut für Neurobiochemie, Medizinische Fakultät der Otto-von-Guericke-Universität Magdeburg, Leipziger Straße 44, D-39120, Magdeburg, Germany, e-mail:

About the authors

Rolf Stricker

Rolf Stricker studied Biochemistry at the University of Tübingen, and graduated in 1992. In 1996 he received his PhD in Biochemistry at the Institute of Physiological Chemistry of the University of Tübingen. From 1994 to March 2014 he worked at the Institute of Neurobiochemistry of the Otto-von-Guericke University, Magdeburg as postdoctoral fellow. Since April 2014 he is a member of the Institute for Biochemistry and Cell Biology of the Otto-von-Guericke University, Magdeburg.

Georg Reiser

Georg Reiser did his PhD at the Max-Planck Institute of Biochemistry in Martinsried and the Ludwig-Maximilians University in Munich under the supervision of B. Hamprecht in the department of F. Lynen. After working as research fellow in the Institute for Physiological Chemistry in Wurzburg, he obtained a DFG-fellowship with further training in electrophysiology at the University College London, Department of Biophysics under R. Miledi. There, he studied nicotinic acetylcholine receptor ion channels. From 1984 he continued research in mechanisms of neural molecular signaling, focusing on calcium regulation and identification of the inositol(1,3,4,5)P4 receptor protein, designated p42IP4. From 1994 he is professor for biochemistry and neurochemistry in Magdeburg, Medical Faculty with research on molecular mechanisms of neuroprotection in ischemia and stroke, covering functions of mitochondria, protease-activated receptors, P2Y nucleotide receptors, nuclear Peroxisome Proliferators Activated Receptors, and iPLA2 isoforms in neurodegenerative diseases.

Acknowledgments

The work in the authors’ laboratory has been supported by grants from BMBF, DFG, and Land Sachsen-Anhalt. The contributing author especially thanks to all his collaborators, who made substantial efforts to elucidate over the years the properties and functions of ADAP1 (p42IP4), Frédéric Donié, Eckehard Hülser, Ute Kunzelmann, Michael Aggensteiner, Fariba Sedehizade, Andrea Haase, and Theo Hanck.

References

Abdelmohsen, K., and Gorospe, M. (2012). RNA-binding protein nucleolin in disease. RNA Biol. 9, 799–808.10.4161/rna.19718Suche in Google Scholar

Aggensteiner, M., and Reiser, G. (2003). Expression of the brain-specific membrane adapter protein p42IP4/centaurin α, a Ins(1,3,4,5)P4/PtdIns(3,4,5)P3 binding protein, in developing rat brain. Brain. Res. Dev. Brain Res. 142, 77–87.10.1016/S0165-3806(03)00033-6Suche in Google Scholar

Aggensteiner, M., Stricker, R., and Reiser, G. (1998). Identification of rat brain p42IP4, a high-affinity inositol(1,3,4,5)tetrakisphosphate/phosphatidylinositol(3,4,5)trisphosphate binding protein. Biochim. Biophys. Acta 1387, 117–128.10.1016/S0167-4838(98)00113-7Suche in Google Scholar

Arimura, N., and Kaibuchi, K. (2007). Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat. Rev. Neurosci. 8, 194–205.10.1038/nrn2056Suche in Google Scholar PubMed

Azarashvili, T., Stricker, R., and Reiser, G. (2010). The mitochondria permeability transition pore complex in the brain with interacting proteins – promising targets for protection in neurodegenerative diseases. Biol. Chem. 391, 619–629.10.1515/bc.2010.070Suche in Google Scholar PubMed

Barnes, A.P., and Polleux, F. (2009). Establishment of axon-dendrite polarity in developing neurons. Annu. Rev. Neurosci. 32, 347–381.10.1146/annurev.neuro.31.060407.125536Suche in Google Scholar PubMed PubMed Central

Barrett, L.E., Van Bockstaele, E.J., Sul, J.Y., Takano, H., Haydon, P.G., and Eberwine, J.H. (2006). Elk-1 associates with the mitochondrial permeability transition pore complex in neurons. Proc. Natl. Acad. Sci. USA 103, 5155–5160.10.1073/pnas.0510477103Suche in Google Scholar PubMed PubMed Central

Bernstein, H.G., Stricker, R., Dobrowolny, H., Trübner, K., Bogerts, B., and Reiser, G. (2007). Histochemical evidence for wide expression of the metalloendopeptidase nardilysin in human brain neurons. Neuroscience 146, 1513–1523.10.1016/j.neuroscience.2007.02.057Suche in Google Scholar PubMed

Blanpied, T.A., and Ehlers, M.D. (2004). Microanatomy of dendritic spines: emerging principles of synaptic pathology in psychiatric and neurological disease. Biol. Psych. 55, 1121–1127.10.1016/j.biopsych.2003.10.006Suche in Google Scholar PubMed

Borrmann, C., Stricker, R., and Reiser, G. (2011a). Retinoic acid-induced upregulation of the metalloendopeptidase nardilysin is accelerated by co-expression of the brain-specific protein p42IP4 (centaurin α1; ADAP1) in neuroblastoma cells. Neurochem. Int. 59, 936–944.10.1016/j.neuint.2011.07.004Suche in Google Scholar PubMed

Borrmann, C., Stricker, R., and Reiser, G. (2011b). Tubulin potentiates the interaction of the metalloendopeptidase nardilysin with the neuronal scaffold protein p42IP4/centaurin-α1 (ADAP1). Cell Tissue Res. 346, 89–98.10.1007/s00441-011-1245-zSuche in Google Scholar

Bos, J.L., Rehmann, H., and Wittinghofer, A. (2007). GEFs and GAPs: critical elements in the control of small G proteins. Cell 129, 865–877.10.1016/j.cell.2007.05.018Suche in Google Scholar

Campa, F., and Randazzo, P.A. (2008). Arf GTPase-activating proteins and their potential role in cell migration and invasion. Cell. Adh. Migr. 2, 258–262.10.4161/cam.2.4.6959Suche in Google Scholar

Casanova, J.E. (2007). Regulation of Arf activation: the Sec7 family of guanine nucleotide exchange factors. Traffic 8, 1476–1485.10.1111/j.1600-0854.2007.00634.xSuche in Google Scholar

Chanda, S.K., White, S., Orth, A.P., Reisdorph, R., Miraglia, L., Thomas, R.S., DeJesus, P., Mason, D.E., Huang, Q., Vega, R., et al. (2003). Genome-scale functional profiling of the mammalian AP-1 signaling pathway. Proc. Natl. Acad. Sci. USA 100, 12153–12158.10.1073/pnas.1934839100Suche in Google Scholar

Chow, K.M., Ma, Z., Cai, J., Pierce, W.M., and Hersh, L.B. (2005). Nardilysin facilitates complex formation between mitochondrial malate dehydrogenase and citrate synthase. Biochim. Biophys. Acta 1723, 292–301.10.1016/j.bbagen.2005.02.010Suche in Google Scholar

D’Souza-Schorey, C., and Chavrier, P. (2006). ARF proteins: roles in membrane traffic and beyond. Nature reviews. Molecular Cell. Biol. 7, 347–358.Suche in Google Scholar

Devreotes, P., and Janetopoulos, C. (2003). Eukaryotic chemotaxis: distinctions between directional sensing and polarization. J. Biol. Chem. 278, 20445–20448.10.1074/jbc.R300010200Suche in Google Scholar

Dubois, T., Kerai, P., Zemlickova, E., Howell, S., Jackson, T.R., Venkateswarlu, K., Cullen, P.J., Theibert, A.B., Larose, L., Roach, P.J., et al. (2001). Casein kinase I associates with members of the centaurin-α family of phosphatidylinositol 3,4,5-trisphosphate-binding proteins. J. Biol. Chem. 276, 18757–18764.10.1074/jbc.M010005200Suche in Google Scholar

Dubois, T., Howell, S., Zemlickova, E., and Aitken, A. (2002). Identification of casein kinase Iα interacting protein partners. FEBS Lett. 517, 167–171.10.1016/S0014-5793(02)02614-5Suche in Google Scholar

Dubois, T., Zemlickova, E., Howell, S., and Aitken, A. (2003). Centaurin-α1 associates in vitro and in vivo with nucleolin. Biochem. Biophys. Res. Commun. 301, 502–508.10.1016/S0006-291X(02)03010-3Suche in Google Scholar

East, M.P., and Kahn, R.A. (2011). Models for the functions of Arf GAPs. Sem. Cell Dev. Biol. 22, 3–9.10.1016/j.semcdb.2010.07.002Suche in Google Scholar

Eferl, R., and Wagner, E.F. (2003). AP-1: a double-edged sword in tumorigenesis. Nat. Rev. Cancer 3, 859–868.10.1038/nrc1209Suche in Google Scholar

Fenner, B.J., Scannell, M., and Prehn, J.H. (2010). Expanding the substantial interactome of NEMO using protein microarrays. PLoS One 5, e8799.10.1371/journal.pone.0008799Suche in Google Scholar

Fish, K.J., Cegielska, A., Getman, M.E., Landes, G.M., and Virshup, D.M. (1995). Isolation and characterization of human casein kinase I ε (CKI), a novel member of the CKI gene family. J. Biol. Chem. 270, 14875–14883.10.1074/jbc.270.25.14875Suche in Google Scholar

Flajolet, M., He, G., Heiman, M., Lin, A., Nairn, A.C., and Greengard, P. (2007). Regulation of Alzheimer’s disease amyloid-β formation by casein kinase I. Proc. Natl. Acad. Sci. USA 104, 4159–4164.10.1073/pnas.0611236104Suche in Google Scholar

Galvita, A., Grachev, D., Azarashvili, T., Baburina, Y., Krestinina, O., Stricker, R., and Reiser, G. (2009). The brain-specific protein, p42IP4 (ADAP1) is localized in mitochondria and involved in regulation of mitochondrial Ca2+. J. Neurochem. 109, 1701–1713.10.1111/j.1471-4159.2009.06089.xSuche in Google Scholar

Geraldo, S., and Gordon-Weeks, P.R. (2009). Cytoskeletal dynamics in growth-cone steering. J. Cell Sci. 122, 3595–3604.10.1242/jcs.042309Suche in Google Scholar

Gillingham, A.K., and Munro, S. (2007). The small G proteins of the Arf family and their regulators. Annu. Rev. Cell Dev. Biol. 23, 579–611.10.1146/annurev.cellbio.23.090506.123209Suche in Google Scholar

Ginisty, H., Sicard, H., Roger, B., and Bouvet, P. (1999). Structure and functions of nucleolin. J. Cell Sci. 112, 761–772.10.1242/jcs.112.6.761Suche in Google Scholar

Goldberg, J. (1999). Structural and functional analysis of the ARF1-ARFGAP complex reveals a role for coatomer in GTP hydrolysis. Cell 96, 893–902.10.1016/S0092-8674(00)80598-XSuche in Google Scholar

Goldfinger, L.E. (2008). Choose your own path: specificity in Ras GTPase signaling. Mol. Biosyst. 4, 293–299.10.1039/b716887jSuche in Google Scholar

Gross, S.D., and Anderson, R.A. (1998). Casein kinase I: spatial organization and positioning of a multifunctional protein kinase family. Cell Signal. 10, 699–711.10.1016/S0898-6568(98)00042-4Suche in Google Scholar

Haase, A., Nordmann, C., Sedehizade, F., Borrmann, C., and Reiser, G. (2008). RanBPM, a novel interaction partner of the brain-specific protein p42IP4/centaurin α-1. J. Neurochem. 105, 2237–2248.10.1111/j.1471-4159.2008.05308.xSuche in Google Scholar PubMed

Hammonds-Odie, L.P., Jackson, T.R., Profit, A.A., Blader, I.J., Turck, C.W., Prestwich, G.D., and Theibert, A.B. (1996). Identification and cloning of centaurin-α. A novel phosphatidylinositol 3,4,5-trisphosphate-binding protein from rat brain. J. Biol. Chem. 271, 18859–18868.10.1074/jbc.271.31.18859Suche in Google Scholar PubMed PubMed Central

Hanada, T., Lin, L., Tibaldi, E.V., Reinherz, E.L., and Chishti, A.H. (2000). GAKIN, a novel kinesin-like protein associates with the human homologue of the Drosophila discs large tumor suppressor in T lymphocytes. J. Biol. Chem. 275, 28774–28784.10.1074/jbc.M000715200Suche in Google Scholar PubMed

Hanck, T., Stricker, R., Krishna, U.M., Falck, J.R., Chang, Y.T., Chung, S.K., and Reiser, G. (1999). Recombinant p42IP4, a brain-specific 42-kDa high-affinity Ins(1,3,4,5)P4 receptor protein, specifically interacts with lipid membranes containing Ptd-Ins(3,4,5)P3. Eur. J. Biochem. 261, 577–584.10.1046/j.1432-1327.1999.00326.xSuche in Google Scholar PubMed

Hanck, T., Stricker, R., Sedehizade, F., and Reiser, G. (2004). Identification of gene structure and subcellular localization of human centaurin α2, and p42IP4, a family of two highly homologous, Ins 1,3,4,5-P4-/PtdIns 3,4,5-P3-binding, adapter proteins. J. Neurochem. 88, 326–336.10.1046/j.1471-4159.2003.02143.xSuche in Google Scholar PubMed

Hanger, D.P., Byers, H.L., Wray, S., Leung, K.Y., Saxton, M.J., Seereeram, A., Reynolds, C.H., Ward, M.A., and Anderton, B.H. (2007). Novel phosphorylation sites in tau from Alzheimer brain support a role for casein kinase 1 in disease pathogenesis. J. Biol. Chem. 282, 23645–23654.10.1074/jbc.M703269200Suche in Google Scholar PubMed

Harada, T., Matsuzaki, O., Hayashi, H., Sugano, S., Matsuda, A., and Nishida, E. (2003). AKRL1 and AKRL2 activate the JNK pathway. Genes Cells 8, 493–500.10.1046/j.1365-2443.2003.00650.xSuche in Google Scholar PubMed

Hawadle, M.A., Folarin, N., Martin, R., and Jackson, T.R. (2002). Cytohesins and centaurins control subcellular trafficking of macromolecular signaling complexes: regulation by phosphoinositides and ADP-ribosylation factors. Biol. Res. 35, 247–265.10.4067/S0716-97602002000200017Suche in Google Scholar

Hayashi, H., Matsuzaki, O., Muramatsu, S., Tsuchiya, Y., Harada, T., Suzuki, Y., Sugano, S., Matsuda, A., and Nishida, E. (2006). Centaurin-α1 is a phosphatidylinositol 3-kinase-dependent activator of ERK1/2 mitogen-activated protein kinases. J. Biol. Chem. 281, 1332–1337.10.1074/jbc.M505905200Suche in Google Scholar

Hermosura, M.C., Takeuchi, H., Fleig, A., Riley, A.M., Potter, B.V., Hirata, M., and Penner, R. (2000). InsP4 facilitates store-operated calcium influx by inhibition of InsP3 5-phosphatase. Nature 408, 735–740.10.1038/35047115Suche in Google Scholar

Hernandez-Deviez, D.J., Casanova, J.E., and Wilson, J.M. (2002). Regulation of dendritic development by the ARF exchange factor ARNO. Nat. Neurosci. 5, 623–624.10.1038/nn865Suche in Google Scholar

Hernandez-Deviez, D.J., Roth, M.G., Casanova, J.E., and Wilson, J.M. (2004). ARNO and ARF6 regulate axonal elongation and branching through downstream activation of phosphatidylinositol 4-phosphate 5-kinase α. Mol. Biol. Cell 15, 111–120.10.1091/mbc.e03-06-0410Suche in Google Scholar

Hirokawa, N., Noda, Y., Tanaka, Y., and Niwa, S. (2009). Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol. 10, 682–696.10.1038/nrm2774Suche in Google Scholar

Horiguchi, K., Hanada, T., Fukui, Y., and Chishti, A.H. (2006). Transport of PIP3 by GAKIN, a kinesin-3 family protein, regulates neuronal cell polarity. J. Cell Biol. 174, 425–436.10.1083/jcb.200604031Suche in Google Scholar

Hospital, V., and Prat, A. (2004). Nardilysin, a basic residues specific metallopeptidase that mediates cell migration and proliferation. Protein Pept. Lett. 11, 501–508.10.2174/0929866043406508Suche in Google Scholar

Hunzicker-Dunn, M., Gurevich, V.V., Casanova, J.E., and Mukherjee, S. (2002). ARF6: a newly appreciated player in G protein-coupled receptor desensitization. FEBS Lett. 521, 3–8.10.1016/S0014-5793(02)02822-3Suche in Google Scholar

Isakoff, S.J., Cardozo, T., Andreev, J., Li, Z., Ferguson, K.M., Abagyan, R., Lemmon, M.A., Aronheim, A., and Skolnik, E.Y. (1998). Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast. EMBO J. 17, 5374–5387.10.1093/emboj/17.18.5374Suche in Google Scholar PubMed PubMed Central

Jenne, D.E., Tinschert, S., Reimann, H., Lasinger, W., Thiel, G., Hameister, H., and Kehrer-Sawatzki, H. (2001). Molecular characterization and gene content of breakpoint boundaries in patients with neurofibromatosis type 1 with 17q11.2 microdeletions. Am. J. Hum. Genet. 69, 516–527.10.1086/323043Suche in Google Scholar PubMed PubMed Central

Jia, Y., Subramanian, K.K., Erneux, C., Pouillon, V., Hattori, H., Jo, H., You, J., Zhu, D., Schurmans, S., and Luo, H.R. (2007). Inositol 1,3,4,5-tetrakisphosphate negatively regulates phosphatidylinositol-3,4,5- trisphosphate signaling in neutrophils. Immunity 27, 453–467.10.1016/j.immuni.2007.07.016Suche in Google Scholar

Kahn, R.A., Bruford, E., Inoue, H., Logsdon, J.M., Jr., Nie, Z., Premont, R.T., Randazzo, P.A., Satake, M., Theibert, A.B., Zapp, M.L., et al. (2008). Consensus nomenclature for the human ArfGAP domain-containing proteins. J. Cell. Biol. 182, 1039–1044.10.1083/jcb.200806041Suche in Google Scholar

Kalscheuer, V.M., Musante, L., Fang, C., Hoffmann, K., Fuchs, C., Carta, E., Deas, E., Venkateswarlu, K., Menzel, C., Ullmann, R., et al. (2009). A balanced chromosomal translocation disrupting ARHGEF9 is associated with epilepsy, anxiety, aggression, and mental retardation. Hum. Mutat. 30, 61–68.10.1002/humu.20814Suche in Google Scholar

Kanamarlapudi, V. (2005). Centaurin-α1 and KIF13B kinesin motor protein interaction in ARF6 signalling. Biochem. Soc. Trans. 33, 1279–1281.10.1042/BST0331279Suche in Google Scholar

Kannanayakal, T.J., Tao, H., Vandre, D.D., and Kuret, J. (2006). Casein kinase-1 isoforms differentially associate with neurofibrillary and granulovacuolar degeneration lesions. Acta Neuropathol. 111, 413–421.10.1007/s00401-006-0049-9Suche in Google Scholar

Koo, T.H., Eipper, B.A., and Donaldson, J.G. (2007). Arf6 recruits the Rac GEF Kalirin to the plasma membrane facilitating Rac activation. BMC Cell Biol. 8, 29.10.1186/1471-2121-8-29Suche in Google Scholar

Kreutz, M.R., Böckers, T.M., Sabel, B.A., Hülser, E., Stricker, R., and Reiser, G. (1997a). Expression and subcellular localization of p42IP4/centaurin-α, a brain-specific, high-affinity receptor for inositol 1,3,4,5-tetrakisphosphate and phosphatidylinositol 3,4,5-trisphosphate in rat brain. Eur. J. Neurosci. 9, 2110–2124.10.1111/j.1460-9568.1997.tb01378.xSuche in Google Scholar

Kreutz, M.R., Böckers, T.M., Sabel, B.A., Stricker, R., Hülser, E., and Reiser, G. (1997b). Localization of a 42-kDa inositol 1,3,4,5-tetrakisphosphate receptor protein in retina and change in expression after optic nerve injury. Brain Res. Mol. Brain Res. 45, 283–293.10.1016/S0169-328X(96)00264-1Suche in Google Scholar

Kroemer, G., Galluzzi, L., and Brenner, C. (2007). Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87, 99–163.10.1152/physrev.00013.2006Suche in Google Scholar PubMed

Lakshmana, M.K., Yoon, I.S., Chen, E., Bianchi, E., Koo, E.H., and Kang, D.E. (2009). Novel role of RanBP9 in BACE1 processing of APP and amyloid β peptide generation. J. Biol. Chem. 284, 11863–11872.10.1074/jbc.M807345200Suche in Google Scholar PubMed PubMed Central

Lakshmana, M.K., Chung, J.Y., Wickramarachchi, S., Tak, E., Bianchi, E., Koo, E.H., and Kang, D.E. (2010). A fragment of the scaffolding protein RanBP9 is increased in Alzheimer’s disease brains and strongly potentiates amyloid-beta peptide generation. FASEB J. 24, 119–127.10.1096/fj.09-136457Suche in Google Scholar PubMed PubMed Central

Lawrence, J., Mundell, S.J., Yun, H., Kelly, E., and Venkateswarlu, K. (2005). Centaurin-α1, an ADP-ribosylation factor 6 GTPase-activating protein, inhibits β2-adrenoceptor internalization. Mol. Pharmacol. 67, 1822–1828.10.1124/mol.105.011338Suche in Google Scholar PubMed

Lemmon, M.A. (2008). Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9, 99–111.10.1038/nrm2328Suche in Google Scholar PubMed

Lemmon, M.A., and Ferguson, K.M. (2000). Signal-dependent membrane targeting by pleckstrin homology (PH) domains. Biochem. J. 350, 1–18.10.1042/bj3500001Suche in Google Scholar

Ma, Z., Chow, K.M., Yao, J., and Hersh, L.B. (2004). Nuclear shuttling of the peptidase nardilysin. Arch. Biochem. Biophys. 422, 153–160.10.1016/j.abb.2003.11.024Suche in Google Scholar PubMed

Matsuda, A., Suzuki, Y., Honda, G., Muramatsu, S., Matsuzaki, O., Nagano, Y., Doi, T., Shimotohno, K., Harada, T., Nishida, E., et al. (2003). Large-scale identification and characterization of human genes that activate NF-κB and MAPK signaling pathways. Oncogene 22, 3307–3318.10.1038/sj.onc.1206406Suche in Google Scholar PubMed

McCrea, H.J., and De Camilli, P. (2009). Mutations in phosphoinositide metabolizing enzymes and human disease. Physiology (Bethesda) 24, 8–16.10.1152/physiol.00035.2008Suche in Google Scholar PubMed PubMed Central

Ménager, C., Arimura, N., Fukata, Y., and Kaibuchi, K. (2004). PIP3 is involved in neuronal polarization and axon formation. J. Neurochem. 89, 109–118.10.1046/j.1471-4159.2004.02302.xSuche in Google Scholar PubMed

Miki, H., Okada, Y., and Hirokawa, N. (2005). Analysis of the kinesin superfamily: insights into structure and function. Trends Cell Biol. 15, 467–476.10.1016/j.tcb.2005.07.006Suche in Google Scholar PubMed

Mitin, N., Rossman, K.L., and Der, C.J. (2005). Signaling interplay in Ras superfamily function. Curr. Biol. 15, R563–574.10.1016/j.cub.2005.07.010Suche in Google Scholar PubMed

Moore, C.D., Thacker, E.E., Larimore, J., Gaston, D., Underwood, A., Kearns, B., Patterson, S.I., Jackson, T., Chapleau, C., Pozzo-Miller, L., et al. (2007). The neuronal Arf GAP centaurin α1 modulates dendritic differentiation. J. Cell Sci. 120, 2683–2693.10.1242/jcs.006346Suche in Google Scholar PubMed PubMed Central

Murrin, L.C., and Talbot, J.N. (2007). RanBPM, a scaffolding protein in the immune and nervous systems. J. Neuroimmune Pharmacol. 2, 290–295.10.1007/s11481-007-9079-xSuche in Google Scholar PubMed

Nakata, T., and Hirokawa, N. (2007). Neuronal polarity and the kinesin superfamily proteins. Science STKE 372, pe6.10.1126/stke.3722007pe6Suche in Google Scholar PubMed

Ohno, M., Hiraoka, Y., Lichtenthaler, S.F., Nishi, K., Saijo, S., Matsuoka, T., Tomimoto, H., Araki, W., Takahashi, R., Kita, T., et al. (2014). Nardilysin prevents amyloid plaque formation by enhancing α-secretase activity in an Alzheimer’s disease mouse model. Neurobiol. Aging 35, 213–222.10.1016/j.neurobiolaging.2013.07.014Suche in Google Scholar PubMed

Pasmant, E., Masliah-Planchon, J., Levy, P., Laurendeau, I., Ortonne, N., Parfait, B., Valeyrie-Allanore, L., Leroy, K., Wolkenstein, P., Vidaud, M., et al. (2011). Identification of genes potentially involved in the increased risk of malignancy in NF1-microdeleted patients. Mol. Med. 17, 79–87.10.2119/molmed.2010.00079Suche in Google Scholar PubMed PubMed Central

Peters, P.J., Hsu, V.W., Ooi, C.E., Finazzi, D., Teal, S.B., Oorschot, V., Donaldson, J.G., and Klausner, R.D. (1995). Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments. J. Cell Biol. 128, 1003–1017.10.1083/jcb.128.6.1003Suche in Google Scholar PubMed PubMed Central

Rabiner, C.A., Mains, R.E., and Eipper, B.A. (2005). Kalirin: a dual Rho guanine nucleotide exchange factor that is so much more than the sum of its many parts. Neuroscientist 11, 148–160.10.1177/1073858404271250Suche in Google Scholar PubMed

Randazzo, P.A., and Hirsch, D.S. (2004). Arf GAPs: multifunctional proteins that regulate membrane traffic and actin remodelling. Cell Signal 16, 401–413.10.1016/j.cellsig.2003.09.012Suche in Google Scholar PubMed

Rao, V.R., Corradetti, M.N., Chen, J., Peng, J., Yuan, J., Prestwich, G.D., and Brugge, J.S. (1999). Expression cloning of protein targets for 3-phosphorylated phosphoinositides. J. Biol. Chem. 274, 37893–37900.10.1074/jbc.274.53.37893Suche in Google Scholar PubMed

Rebecchi, M.J., and Scarlata, S. (1998). Pleckstrin homology domains: a common fold with diverse functions. Annu. Rev. Biophys. Biomol. Struct. 27, 503–528.10.1146/annurev.biophys.27.1.503Suche in Google Scholar PubMed

Reiser, G., and Bernstein, H.G. (2002). Neurons and plaques of Alzheimer’s disease patients highly express the neuronal membrane docking protein p42IP4/centaurin α. Neuroreport 13, 2417–2419.10.1097/00001756-200212200-00008Suche in Google Scholar

Reiser, G., and Bernstein, H.G. (2004). Altered expression of protein p42IP4/centaurin-α1 in Alzheimer’s disease brains and possible interaction of p42IP4 with nucleolin. Neuroreport 15, 147–148.10.1097/00001756-200401190-00028Suche in Google Scholar

Reiser, G., Schäfer, R., Donie, F., Hülser, E., Nehls-Sahabandu, M., and Mayr, G.W. (1991). A high-affinity inositol 1,3,4,5-tetrakisphosphate receptor protein from brain is specifically labelled by a newly synthesized photoaffinity analogue, N-(4-azidosalicyl)aminoethanol(1)-1-phospho-D-myo-inositol 3,4,5-trisphosphate. Biochem. J. 280, 533–539.10.1042/bj2800533Suche in Google Scholar

Reiser, G., Striggow, F., Hackmann, C., Schwegler, H., and Yilmazer-Hanke, D.M. (2004). Short-term down-regulation of the brain-specific, PtdIns(3,4,5)P3/Ins(1,3,4,5)P4-binding, adapter protein, p42IP4/centaurin-α 1 in rat brain after acoustic and electric stimulation. Neurochem. Int. 45, 89–93.10.1016/j.neuint.2003.12.003Suche in Google Scholar

Rizzuto, R., De Stefani, D., Raffaello, A., and Mammucari, C. (2012). Mitochondria as sensors and regulators of calcium signalling. Nat. Rev. Mol. Cell. Biol. 13, 566–578.10.1038/nrm3412Suche in Google Scholar

Rodgers, E.E., and Theibert, A.B. (2002). Functions of PI 3-kinase in development of the nervous system. Int. J. Dev. Neurosci. 20, 187–197.10.1016/S0736-5748(02)00047-3Suche in Google Scholar

Rodriguez, O.C., Schaefer, A.W., Mandato, C.A., Forscher, P., Bement, W.M., and Waterman-Storer, C.M. (2003). Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell. Biol. 5, 599–609.10.1038/ncb0703-599Suche in Google Scholar PubMed

Satoh, J., Obayashi, S., Misawa, T., Sumiyoshi, K., Oosumi, K., and Tabunoki, H. (2009). Protein microarray analysis identifies human cellular prion protein interactors. Neuropathol. Appl. Neurobiol. 35, 16–35.10.1111/j.1365-2990.2008.00947.xSuche in Google Scholar PubMed

Sauer, K., and Cooke, M.P. (2010). Regulation of immune cell development through soluble inositol-1,3,4,5-tetrakisphosphate. Nat Rev Immunol 10, 257–271.10.1038/nri2745Suche in Google Scholar PubMed PubMed Central

Schell, M.J. (2010). Inositol trisphosphate 3-kinases: focus on immune and neuronal signaling. Cell. Mol. Life Sci. 67, 1755–1778.10.1007/s00018-009-0238-5Suche in Google Scholar PubMed

Schnack, C., Danzer, K.M., Hengerer, B., and Gillardon, F. (2008). Protein array analysis of oligomerization-induced changes in α-synuclein protein-protein interactions points to an interference with Cdc42 effector proteins. Neurosci. 154, 1450–1457.10.1016/j.neuroscience.2008.02.049Suche in Google Scholar

Schwab, C., DeMaggio, A.J., Ghoshal, N., Binder, L.I., Kuret, J., and McGeer, P.L. (2000). Casein kinase 1 δ is associated with pathological accumulation of tau in several neurodegenerative diseases. Neurobiol. Aging 21, 503–510.10.1016/S0197-4580(00)00110-XSuche in Google Scholar

Sedehizade, F., Hanck, T., Horstmeyer, A., Stricker, R., Bernstein, H.-G., and Reiser, G. (2002). Cellular expression and subcellular localization of the human Ins(1,3,4,5)P4-binding protein, p42IP4, in human brain and in neuronal cells. Brain Res. Mol. Brain Res. 99, 1–11.10.1016/S0169-328X(01)00335-7Suche in Google Scholar

Sedehizade, F., von Klot, C., Hanck, T., and Reiser, G. (2005). p42IP4/centaurin α1, a brain-specific PtdIns(3,4,5)P3/Ins(1,3,4,5)P4-binding protein: membrane trafficking induced by epidermal growth factor is inhibited by stimulation of phospholipase C-coupled thrombin receptor. Neurochem. Res. 30, 1319–1330.10.1007/s11064-005-8804-1Suche in Google Scholar

Seidah, N.G., and Prat, A. (2002). Precursor convertases in the secretory pathway, cytosol and extracellular milieu. Essays Biochem. 38, 79–94.10.1042/bse0380079Suche in Google Scholar

Shaulian, E., and Karin, M. (2002). AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4, E131–136.10.1038/ncb0502-e131Suche in Google Scholar

Soh, U.J., Dores, M.R., Chen, B., and Trejo, J. (2010). Signal transduction by protease-activated receptors. Br. J. Pharmacol. 160, 191–203.10.1111/j.1476-5381.2010.00705.xSuche in Google Scholar

Stricker, R., Hülser, E., Fischer, J., Jarchau, T., Walter, U., Lottspeich, F., and Reiser, G. (1997). cDNA cloning of porcine p42IP4, a membrane-associated and cytosolic 42 kDa inositol(1,3,4,5)tetrakisphosphate receptor from pig brain with similarly high-affinity for phosphatidylinositol (3,4,5)P3. FEBS Lett. 405, 229–236.10.1016/S0014-5793(97)00188-9Suche in Google Scholar

Stricker, R., Adelt, S., Vogel, G., and Reiser, G. (1999). Translocation between membranes and cytosol of p42IP4, a specific inositol 1,3,4,5-tetrakisphosphate/phosphatidylinositol 3,4,5-trisphosphate-receptor protein from brain, is induced by inositol 1,3,4,5-tetrakisphosphate and regulated by a membrane-associated 5-phosphatase. Eur. J. Biochem. 265, 815–824.10.1046/j.1432-1327.1999.00795.xSuche in Google Scholar PubMed

Stricker, R., Chow, K.M., Walther, D., Hanck, T., Hersh, L.B., and Reiser, G. (2006). Interaction of the brain-specific protein p42IP4/centaurin-α1 with the peptidase nardilysin is regulated by the cognate ligands of p42IP4, PtdIns(3,4,5)P3 and Ins(1,3,4,5)P4, with stereospecificity. J. Neurochem. 98, 343–354.10.1111/j.1471-4159.2006.03869.xSuche in Google Scholar PubMed

Suresh, B., Ramakrishna, S., and Baek, K.H. (2012). Diverse roles of the scaffolding protein RanBPM. Drug Discov. Today 17, 379–387.10.1016/j.drudis.2011.10.030Suche in Google Scholar PubMed

Szatmari, E.M., Oliveira, A.F., Sumner, E.J., and Yasuda, R. (2013). Centaurin-α1-Ras-Elk-1 signaling at mitochondria mediates β-amyloid-induced synaptic dysfunction. J. Neurosci. 33, 5367–5374.10.1523/JNEUROSCI.2641-12.2013Suche in Google Scholar PubMed PubMed Central

Tanaka, K., Imajoh-Ohmi, S., Sawada, T., Shirai, R., Hashimoto, Y., Iwasaki, S., Kaibuchi, K., Kanaho, Y., Shirai, T., Terada, Y., et al. (1997). A target of phosphatidylinositol 3,4,5-trisphosphate with a zinc finger motif similar to that of the ADP-ribosylation-factor GTPase-activating protein and two pleckstrin homology domains. Eur. J. Biochem. 245, 512–519.10.1111/j.1432-1033.1997.00512.xSuche in Google Scholar PubMed

Tanaka, K., Horiguchi, K., Yoshida, T., Takeda, M., Fujisawa, H., Takeuchi, K., Umeda, M., Kato, S., Ihara, S., Nagata, S., et al. (1999). Evidence that a phosphatidylinositol 3,4,5-trisphosphate-binding protein can function in nucleus. J. Biol. Chem. 274, 3919–3922.10.1074/jbc.274.7.3919Suche in Google Scholar PubMed

Thacker, E., Kearns, B., Chapman, C., Hammond, J., Howell, A., and Theibert, A. (2004). The Arf6 GAP centaurin α-1 is a neuronal actin-binding protein which also functions via GAP-independent activity to regulate the actin cytoskeleton. Eur. J. Cell Biol. 83, 541–554.10.1078/0171-9335-00416Suche in Google Scholar PubMed

Tong, Y., Tempel, W., Wang, H., Yamada, K., Shen, L., Senisterra, G.A., MacKenzie, F., Chishti, A.H., and Park, H.W. (2010). Phosphorylation-independent dual-site binding of the FHA domain of KIF13 mediates phosphoinositide transport via centaurin α1. Proc. Natl. Acad. Sci. USA 107, 20346–20351.10.1073/pnas.1009008107Suche in Google Scholar PubMed PubMed Central

van Spronsen, M., and Hoogenraad, C.C. (2010). Synapse pathology in psychiatric and neurologic disease. Curr. Neurol. Neurosci. Rep. 10, 207–214.10.1007/s11910-010-0104-8Suche in Google Scholar PubMed PubMed Central

Vanhaesebroeck, B., Leevers, S.J., Ahamadi, K., Timms, J., Katso, R., Driscoll, P.C., Woscholski, R., Parker, P.J., and Waterfield, M.D. (2001). Synthesis and function of 3-phosphorylated inositol lipids. Annu. Rev. Biochem. 70, 535–602.10.1146/annurev.biochem.70.1.535Suche in Google Scholar PubMed

Venkateswarlu, K., and Cullen, P.J. (1999). Molecular cloning and functional characterization of a human homologue of centaurin-α. Biochem. Biophys. Res. Commun. 262, 237–244.10.1006/bbrc.1999.1065Suche in Google Scholar PubMed

Venkateswarlu, K., Oatey, P.B., Tavare, J.M., Jackson, T.R., and Cullen, P.J. (1999). Identification of centaurin-α1 as a potential in vivo phosphatidylinositol 3,4,5-trisphosphate-binding protein that is functionally homologous to the yeast ADP-ribosylation factor (ARF) GTPase-activating protein, Gcs1. Biochem. J. 340, 359–363.10.1042/bj3400359Suche in Google Scholar

Venkateswarlu, K., Brandom, K.G., and Lawrence, J.L. (2004). Centaurin-α1 is an in vivo phosphatidylinositol 3,4,5-trisphosphate-dependent GTPase-activating protein for ARF6 that is involved in actin cytoskeleton organization. J. Biol. Chem. 279, 6205–6208.10.1074/jbc.C300482200Suche in Google Scholar

Venkateswarlu, K., Hanada, T., and Chishti, A.H. (2005). Centaurin-α1 interacts directly with kinesin motor protein KIF13B. J. Cell Sci. 118, 2471–2484.10.1242/jcs.02369Suche in Google Scholar

Venkateswarlu, K., Brandom, K.G., and Yun, H. (2007). PI-3-kinase-dependent membrane recruitment of centaurin-α2 is essential for its effect on ARF6-mediated actin cytoskeleton reorganisation. J. Cell Sci. 120, 792–801.10.1242/jcs.03373Suche in Google Scholar

Venturin, M., Guarnieri, P., Natacci, F., Stabile, M., Tenconi, R., Clementi, M., Hernandez, C., Thompson, P., Upadhyaya, M., Larizza, L., et al. (2004). Mental retardation and cardiovascular malformations in NF1 microdeleted patients point to candidate genes in 17q11.2. J. Med. Genet. 41, 35–41.10.1136/jmg.2003.014761Suche in Google Scholar

Venturin, M., Bentivegna, A., Moroni, R., Larizza, L., and Riva, P. (2005). Evidence by expression analysis of candidate genes for congenital heart defects in the NF1 microdeletion interval. Ann. Hum. Genet. 69, 508–516.10.1111/j.1529-8817.2005.00203.xSuche in Google Scholar

Wennerberg, K., Rossman, K.L., and Der, C.J. (2005). The Ras superfamily at a glance. J. Cell Sci. 118, 843–846.10.1242/jcs.01660Suche in Google Scholar

Whitley, P., Gibbard, A.M., Koumanov, F., Oldfield, S., Kilgour, E.E., Prestwich, G.D., and Holman, G.D. (2002). Identification of centaurin-α2: a phosphatidylinositide-binding protein present in fat, heart and skeletal muscle. Eur. J. Cell Biol. 81, 222–230.10.1078/0171-9335-00242Suche in Google Scholar

Yamada, K.H., Hanada, T., and Chishti, A.H. (2007). The effector domain of human Dlg tumor suppressor acts as a switch that relieves autoinhibition of kinesin-3 motor GAKIN/KIF13B. Biochemistry 46, 10039–10045.10.1021/bi701169wSuche in Google Scholar

Yoshimura, Y., Yamauchi, Y., Shinkawa, T., Taoka, M., Donai, H., Takahashi, N., Isobe, T., and Yamauchi, T. (2004). Molecular constituents of the postsynaptic density fraction revealed by proteomic analysis using multidimensional liquid chromatography-tandem mass spectrometry. J. Neurochem. 88, 759–768.10.1046/j.1471-4159.2003.02136.xSuche in Google Scholar

Zemlickova, E., Dubois, T., Kerai, P., Clokie, S., Cronshaw, A.D., Wakefield, R.I., Johannes, F.J., and Aitken, A. (2003). Centaurin-α1 associates with and is phosphorylated by isoforms of protein kinase C. Biochem. Biophys. Res. Commun. 307, 459–465.10.1016/S0006-291X(03)01187-2Suche in Google Scholar

Zuccotti, P., Cartelli, D., Stroppi, M., Pandini, V., Venturin, M., Aliverti, A., Battaglioli, E., Cappelletti, G., and Riva, P. (2012). Centaurin-α2 interacts with β-tubulin and stabilizes microtubules. PLoS One 7, e52867.10.1371/journal.pone.0052867Suche in Google Scholar PubMed PubMed Central

Received: 2014-1-21
Accepted: 2014-4-16
Published Online: 2014-4-23
Published in Print: 2014-11-1

©2014 by De Gruyter

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