Lipid binding defects and perturbed synaptogenic activity of a collybistin R290H mutant that causes epilepsy and intellectual disability

Journal of Biological Chemistry

Volumn 290, Issue 13, 2015, Pages 8256-8270

  Papadopoulos, Theofilos ^a   Schemm, Rudolf ^b   Grubmüller, Helmut ^b   Brose, Nils ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

INTELLECTUAL DISABILITY; LIPID BINDING; MENTAL RETARDATION; NEW MECHANISMS; SYNAPTOGENESIS;

NEUROLOGY;

ARGININE; COLLYBISTIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; HISTIDINE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; UNCLASSIFIED DRUG; ARHGEF9 PROTEIN, HUMAN; CARRIER PROTEIN; GEPHYRIN; MEMBRANE PROTEIN; POLYPHOSPHOINOSITIDE; PROTEIN BINDING; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHOQ PROTEIN, HUMAN;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; EMBRYO; EPILEPSY; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; INTELLECTUAL IMPAIRMENT; MEMBRANE BINDING; MISSENSE MUTATION; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOUSE; MUTANT; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; RAT; SYNAPTOGENESIS; AMINO ACID SEQUENCE; ANIMAL; CELL MEMBRANE; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; GENETIC ASSOCIATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; PROTEIN TRANSPORT; SYNAPSE;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; EPILEPSY; GENETIC ASSOCIATION STUDIES; INTELLECTUAL DISABILITY; MEMBRANE PROTEINS; MICE; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; RATS; RHO GTP-BINDING PROTEINS; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS; SYNAPSES;

EID: 84925813811     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.633024     Document Type: Article

References (44)

1. Luscher, B., Fuchs, T., and Kilpatrick, C. L. (2011) GABAA receptor trafficking- mediated plasticity of inhibitory synapses. Neuron 70, 385-409
2. Smith, K. R., and Kittler, J. T. (2010) The cell biology of synaptic inhibition in health and disease. Curr. Opin. Neurobiol. 20, 550-556
3. Ramamoorthi, K., and Lin, Y. (2011) The contribution of GABAergic dysfunction to neurodevelopmental disorders. Trends Mol. Med. 17, 452-462
4. Verpelli, C., Galimberti, I., Gomez-Mancilla, B., and Sala, C. (2014) Molecular basis for prospective pharmacological treatment strategies in intellectual disability syndromes. Dev. Neurobiol. 74, 197-206
5. Papadopoulos, T., and Soykan, T. (2011) The role of collybistin in gephyrin clustering at inhibitory synapses: facts and open questions. Front. Cell. Neurosci. 5, 11
6. Papadopoulos, T., Korte, M., Eulenburg, V., Kubota, H., Retiounskaia, M., Harvey, R. J., Harvey, K., O'Sullivan, G. A., Laube, B., Hülsmann, S., Geiger, J. R., and Betz, H. (2007) Impaired GABAergic transmission and altered hippocampal synaptic plasticity in collybistin-deficient mice. EMBO J. 26, 3888-3899
7. Harvey, K., Duguid, I. C., Alldred, M. J., Beatty, S. E., Ward, H., Keep, N. H., Lingenfelter, S. E., Pearce, B. R., Lundgren, J., Owen, M. J., Smart, T. G., Lüscher, B., Rees, M. I., and Harvey, R. J. (2004) The GDP-GTP exchange factor collybistin: An essential determinant of neuronal gephyrin clustering. J. Neurosci. 24, 5816-5826
8. Marco, E. J., Abidi, F. E., Bristow, J., Dean, W. B., Cotter, P., Jeremy, R. J., Schwartz, C. E., and Sherr, E. H. (2008) ARHGEF9 disruption in a female patient is associated with X linked mental retardation and sensory hyperarousal. J. Med. Genet. 45, 100-105
9. Kalscheuer, V. M., Musante, L., Fang, C., Hoffmann, K., Fuchs, C., Carta, E., Deas, E., Venkateswarlu, K., Menzel, C., Ullmann, R., Tommerup, N., Dalprà, L., Tzschach, A., Selicorni, A., Lüscher, B., Ropers, H. H., Harvey, K., and Harvey, R. J. (2009) A balanced chromosomal translocation disrupting ARHGEF9 is associated with epilepsy, anxiety, aggression, and mental retardation. Hum. Mutat. 30, 61-68
10. Lesca, G., Till, M., Labalme, A., Vallee, D., Hugonenq, C., Philip, N., Edery, P., and Sanlaville, D. (2011) De novo Xq11.11 microdeletion including ARHGEF9 in a boy with mental retardation, epilepsy, macrosomia, and dysmorphic features. Am. J. Med. Genet. 155A, 1706-1711
11. Shimojima, K., Sugawara, M., Shichiji, M., Mukaida, S., Takayama, R., Imai, K., and Yamamoto, T. (2011) Loss-of-function mutation of collybistin is responsible for X-linked mental retardation associated with epilepsy. J. Hum. Genet. 56, 561-565
12. Lemke, J. R., Riesch, E., Scheurenbrand, T., Schubach, M., Wilhelm, C., Steiner, I., Hansen, J., Courage, C., Gallati, S., Bürki, S., Strozzi, S., Simonetti, B. G., Grunt, S., Steinlin, M., Alber, M., Wolff, M., Klopstock, T., Prott, E. C., Lorenz, R., Spaich, C., Rona, S., Lakshminarasimhan, M., Kröll, J., Dorn, T., Krämer, G., Synofzik, M., Becker, F., Weber, Y. G., Lerche, H., Böhm, D., and Biskup, S. (2012) Targeted next generation sequencing as a diagnostic tool in epileptic disorders. Epilepsia 53, 1387-1398
13. de Ligt, J., Willemsen, M. H., van Bon, B. W., Kleefstra, T., Yntema, H. G., Kroes, T., Vulto-van Silfhout, A. T., Koolen, D. A., de Vries, P., Gilissen, C., del Rosario, M., Hoischen, A., Scheffer, H., de Vries, B. B., Brunner, H. G., Veltman, J. A., and Vissers, L. E. (2012) Diagnostic exome sequencing in persons with severe intellectual disability. N. Engl. J. Med. 367, 1921-1929
14. Soykan, T., Schneeberger, D., Tria, G., Buechner, C., Bader, N., Svergun, D., Tessmer, I., Poulopoulos, A., Papadopoulos, T., Varoqueaux, F., Schindelin, H., and Brose, N. (2014) A conformational switch in collybistin determines the differentiation of inhibitory postsynapses. EMBO J. 33, 2113-2133
15. Reid, T., Bathoorn, A., Ahmadian, M. R., and Collard, J. G. (1999) Identification and characterization of hPEM-2, a guanine nucleotide exchange factor specific for Cdc42. J. Biol. Chem. 274, 33587-33593
16. Mayer, S., Kumar, R., Jaiswal, M., Soykan, T., Ahmadian, M. R., Brose, N., Betz, H., Rhee, J. S., and Papadopoulos, T. (2013) Collybistin activation by GTP-TC10 enhances postsynaptic gephyrin clustering and hippocampal GABAergic neurotransmission. Proc. Natl. Acad. Sci. U.S.A. 110, 20795-20800
17. Reddy-Alla, S., Schmitt, B., Birkenfeld, J., Eulenburg, V., Dutertre, S., Böhringer, C., Götz, M., Betz, H., and Papadopoulos, T. (2010) PH-domain- driven targeting of collybistin but not Cdc42 activation is required for synaptic gephyrin clustering. Eur. J. Neurosci. 31, 1173-1184
18. Kins, S., Betz, H., and Kirsch, J. (2000) Collybistin, a newly identified brainspecific GEF, induces submembrane clustering of gephyrin. Nat. Neurosci. 3, 22-29
19. Poulopoulos, A., Aramuni, G., Meyer, G., Soykan, T., Hoon, M., Papadopoulos, T., Zhang, M., Paarmann, I., Fuchs, C., Harvey, K., Jedlicka, P., Schwarzacher, S. W., Betz, H., Harvey, R. J., Brose, N., Zhang, W., and Varoqueaux, F. (2009) Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63, 628-642
20. Fuhrmann, J. C., Kins, S., Rostaing, P., El Far, O., Kirsch, J., Sheng, M., Triller, A., Betz, H., and Kneussel, M. (2002) Gephyrin interacts with dynein light chains 1 and 2, components of motor protein complexes. J. Neurosci. 22, 5393-5402
21. Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., and Berendsen, H. J. (2005) GROMACS: fast, flexible, and free. J. Comput. Chem. 26, 1701-1718
22. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 4, 435-447
23. Pronk, S., Páll, S., Schulz, R., Larsson, P., Bjelkmar, P., Apostolov, R., Shirts, M. R., Smith, J. C., Kasson, P. M., van der Spoel, D., Hess, B., and Lindahl, E. (2013) GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29, 845-854
24. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712-725
25. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935
26. Darden, T. A., and Pedersen, L. G. (1993) Molecular modeling: an experimental tool. Environ. Health Perspect. 101, 410-412
27. Bussi, G., Donadio, D., and Parrinello, M. (2007) Canonical sampling through velocity rescaling. J. Chem. Phys. 126, 014101
28. Berendsen, H. J. C., Postma, J. P. M., Vangunsteren, W. F., Dinola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690
29. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997) LINCS: A linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463-1472
30. Xiang, S., Kim, E. Y., Connelly, J. J., Nassar, N., Kirsch, J., Winking, J., Schwarz, G., and Schindelin, H. (2006) The crystal structure of Cdc42 in complex with collybistin II, a gephyrin-interacting guanine nucleotide exchange factor. J. Mol. Biol. 359, 35-46
31. Chiou, T. T., Bonhomme, B., Jin, H., Miralles, C. P., Xiao, H., Fu, Z., Harvey, R. J., Harvey, K., Vicini, S., and De Blas, A. L. (2011) Differential regulation of the postsynaptic clustering of γ-aminobutyric acid type A (GABAA) receptors by collybistin isoforms. J. Biol. Chem. 286, 22456-22468
32. Hemsath, L., Dvorsky, R., Fiegen, D., Carlier, M. F., and Ahmadian, M. R. (2005) An electrostatic steering mechanism of Cdc42 recognition by Wiskott- Aldrich syndrome proteins. Mol. Cell 20, 313-324
33. Neudauer, C. L., Joberty, G., Tatsis, N., and Macara, I. G. (1998) Distinct cellular effects and interactions of the Rho-family GTPase TC10. Curr. Biol. 8, 1151-1160
34. Grosskreutz, Y., Hermann, A., Kins, S., Fuhrmann, J. C., Betz, H., and Kneussel, M. (2001) Identification of a gephyrin-binding motif in the GDP/GTP exchange factor collybistin. Biol. Chem. 382, 1455-1462
35. Tyagarajan, S. K., Ghosh, H., Harvey, K., and Fritschy, J. M. (2011) Collybistin splice variants differentially interact with gephyrin and Cdc42 to regulate gephyrin clustering at GABAergic synapses. J. Cell Sci. 124, 2786-2796
36. Saiepour, L., Fuchs, C., Patrizi, A., Sassoè-Pognetto, M., Harvey, R. J., and Harvey, K. (2010) Complex role of collybistin and gephyrin in GABAA receptor clustering. J. Biol. Chem. 285, 29623-29631
37. Wenk, M. R., and De Camilli, P. (2004) Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc. Natl. Acad. Sci. U.S.A. 101, 8262-8269
38. Man, H. Y., Wang, Q., Lu, W. Y., Ju, W., Ahmadian, G., Liu, L., D'Souza, S., Wong, T. P., Taghibiglou, C., Lu, J., Becker, L. E., Pei, L., Liu, F., Wymann, M. P., MacDonald, J. F., and Wang, Y. T. (2003) Activation of PI3-kinase is required for AMPA receptor insertion during LTP of mEPSCs in cultured hippocampal neurons. Neuron 38, 611-624
39. Gillooly, D. J., Morrow, I. C., Lindsay, M., Gould, R., Bryant, N. J., Gaullier, J. M., Parton, R. G., and Stenmark, H. (2000) Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J. 19, 4577-4588
40. Vicinanza, M., D'Angelo, G., Di Campli, A., and De Matteis, M. A. (2008) Function and dysfunction of the PI system in membrane trafficking. EMBO J. 27, 2457-2470
41. Raiborg, C., Schink, K. O., and Stenmark, H. (2013) Class III phosphatidylinositol 3-kinase and its catalytic product PtdIns3P in regulation of endocytic membrane traffic. FEBS J. 280, 2730-2742
42. Falasca, M., and Maffucci, T. (2006) Emerging roles of phosphatidylinositol 3-monophosphate as a dynamic lipid second messenger. Arch. Physiol. Biochem. 112, 274-284
43. Maffucci, T., Brancaccio, A., Piccolo, E., Stein, R. C., and Falasca, M. (2003) Insulin induces phosphatidylinositol-3-phosphate formation through TC10 activation. EMBO J. 22, 4178-4189
44. Falasca, M., Hughes, W. E., Dominguez, V., Sala, G., Fostira, F., Fang, M. Q., Cazzolli, R., Shepherd, P. R., James, D. E., and Maffucci, T. (2007) The role of phosphoinositide 3-kinase C2alpha in insulin signaling. J. Biol. Chem. 282, 28226-28236