Homodimerization and isoform-specific heterodimerization of neuroligins

Biochemical Journal

Volumn 446, Issue 2, 2012, Pages 321-330

  Poulopoulos, Alexandros ^a,b   Soykan, Tolga ^a   Tuffy, Liam P ^a   Hammer, Matthieu ^a   Varoqueaux, Fréd́erique ^a   Brose, Nils ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Autism; Cross linking; Dimer; Endoplasmic reticulum (ER) retention; Oligomerization; Synaptic adhesion; Transmembrane domain

Indexed keywords

HETERODIMER; HOMODIMER; ISOPROTEIN; NEUROLIGIN; NEUROLIGIN 1; OLIGOMER;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTISM; CELL SURFACE; CROSS LINKING; DIMERIZATION; HIPPOCAMPUS; HUMAN; HUMAN CELL; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; QUALITY CONTROL; RAT;

AMINO ACID SUBSTITUTION; ANIMALS; AUTISTIC DISORDER; BRAIN; CELL ADHESION MOLECULES, NEURONAL; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; CRICETINAE; CROSS-LINKING REAGENTS; DIMERIZATION; HEK293 CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MUTANT PROTEINS; NERVE TISSUE PROTEINS; NEURONS; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; RECOMBINANT FUSION PROTEINS; SPINAL CORD;

EID: 84865154636     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120808     Document Type: Article

References (39)

1. Song, J. Y., Ichtchenko, K., Südhof, T. C. and Brose, N. (1999) Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc. Natl. Acad. Sci. U.S.A. 96, 1100-1105 (Pubitemid 29072190)
2. Chubykin, A. A., Atasoy, D., Etherton, M. R., Brose, N., Kavalali, E. T., Gibson, J. R. and Südhof, T. C. (2007) Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 54, 919-931 (Pubitemid 46907504)
3. Hoon, M., Soykan, T., Falkenburger, B., Hammer, M., Patrizi, A., Schmidt, K. F., Sassoe-Pognetto, M., Lowel, S., Moser, T., Taschenberger, H. et al. (2011) Neuroligin-4 is localized to glycinergic postsynapses and regulates inhibition in the retina. Proc. Natl. Acad. Sci. U.S.A. 108, 3053-3058
4. Poulopoulos, A., Aramuni, G., Meyer, G., Soykan, T., Hoon, M., Papadopoulos, T., Zhang, M., Paarmann, I., Fuchs, C., Harvey, K. et al. (2009) Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63, 628-642
5. Varoqueaux, F., Jamain, S. and Brose, N. (2004) Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell Biol. 83, 449-456 (Pubitemid 39433525)
6. Conroy, W. G., Nai, Q., Ross, B., Naughton, G. and Berg, D. K. (2007) Postsynaptic neuroligin enhances presynaptic inputs at neuronal nicotinic synapses. Dev. Biol. 307, 79-91 (Pubitemid 46900818)
7. Ichtchenko, K., Hata, Y., Nguyen, T., Ullrich, B., Missler, M., Moomaw, C. and Südhof, T. C. (1995) Neuroligin 1: a splice site-specific ligand for β-neurexins. Cell 81, 435-443
8. Ichtchenko, K., Nguyen, T. and Südhof, T. C. (1996) Structures, alternative splicing, and neurexin binding of multiple neuroligins. J. Biol. Chem. 271, 2676-2682 (Pubitemid 26047882)
9. Jamain, S., Radyushkin, K., Hammerschmidt, K., Granon, S., Boretius, S., Varoqueaux, F., Ramanantsoa, N., Gallego, J., Ronnenberg, A., Winter, D. et al. (2008) Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc. Natl. Acad. Sci. U.S.A. 105, 1710-1715 (Pubitemid 351346579)
10. Graf, E. R., Zhang, X., Jin, S. X., Linhoff, M. W. and Craig, A. M. (2004) Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119, 1013-1026 (Pubitemid 40037614)
11. Budreck, E. C. and Scheiffele, P. (2007) Neuroligin-3 is a neuronal adhesion protein at GABAergic and glutamatergic synapses. Eur. J. Neurosci. 26, 1738-1748 (Pubitemid 47493212)
12. Dean, C., Scholl, F. G., Choih, J., DeMaria, S., Berger, J., Isacoff, E. and Scheiffele, P. (2003) Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci. 6, 708-716 (Pubitemid 36792885)
13. Comoletti, D., Flynn, R. E., Boucard, A. A., Demeler, B., Schirf, V., Shi, J., Jennings, L. L., Newlin, H. R., Südhof, T. C. and Taylor, P. (2006) Gene selection, alternative splicing, and post-translational processing regulate neuroligin selectivity for β-neurexins. Biochemistry 45, 12816-12827 (Pubitemid 44630868)
14. Comoletti, D., Grishaev, A., Whitten, A. E., Taylor, P. and Trewhella, J. (2008) Characterization of the solution structure of a neuroligin/β- neurexin complex. Chem. Biol. Interact. 175, 150-155
15. Araç, D., Boucard, A. A., Ozkan, E., Strop, P., Newell, E., Südhof, T. C. and Brunger, A. T. (2007) Structures of neuroligin-1 and the neuroligin-1/neurexin-1 β complex reveal specific protein-protein and protein-Ca2+ interactions. Neuron 56, 992-1003 (Pubitemid 350251120)
16. Fabrichny, I. P., Leone, P., Sulzenbacher, G., Comoletti, D., Miller, M. T., Taylor, P., Bourne, Y. and Marchot, P. (2007) Structural analysis of the synaptic protein neuroligin and its β-neurexin complex: determinants for folding and cell adhesion. Neuron 56, 979-991 (Pubitemid 350258607)
17. Koehnke, J., Jin, X., Budreck, E. C., Posy, S., Scheiffele, P., Honig, B. and Shapiro, L. (2008) Crystal structure of the extracellular cholinesterase-like domain from neuroligin-2. Proc. Natl. Acad. Sci. U.S.A. 105, 1873-1878 (Pubitemid 351439432)
18. Levinson, J. N. and El-Husseini, A. (2007) A crystal-clear interaction: relating neuroligin/neurexin complex structure to function at the synapse. Neuron 56, 937-939 (Pubitemid 350251122)
19. Zhang, C., Milunsky, J. M., Newton, S., Ko, J., Zhao, G., Maher, T. A., Tager-Flusberg, H., Bolliger, M. F., Carter, A. S., Boucard, A. A. et al. (2009) A neuroligin-4 missense mutation associated with autism impairs neuroligin-4 folding and endoplasmic reticulum export. J. Neurosci. 29, 10843-10854
20. Brewer, G. J. (1995) Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus. J. Neurosci. Res. 42, 674-683
21. Jedlicka, P., Hoon, M., Papadopoulos, T., Vlachos, A., Winkels, R., Poulopoulos, A., Betz, H., Deller, T., Brose, N., Varoqueaux, F. and Schwarzacher, S. W. (2011) Increased dentate gyrus excitability in neuroligin-2-deficient mice in vivo. Cereb. Cortex 21, 357-367
22. Varoqueaux, F., Aramuni, G., Rawson, R. L., Mohrmann, R., Missler, M., Gottmann, K., Zhang, W., Sudhof, T. C. and Brose, N. (2006) Neuroligins determine synapse maturation and function. Neuron 51, 741-754 (Pubitemid 44374915)
23. Irie, M., Hata, Y., Takeuchi, M., Ichtchenko, K., Toyoda, A., Hirao, K., Takai, Y., Rosahl, T. W. and Südhof, T. C. (1997) Binding of neuroligins to PSD-95. Science 277, 1511-1515 (Pubitemid 27449240)
24. Iida, J., Hirabayashi, S., Sato, Y. and Hata, Y. (2004) Synaptic scaffolding molecule is involved in the synaptic clustering of neuroligin. Mol. Cell. Neurosci. 27, 497-508 (Pubitemid 39540003)
25. Sato, K., Sato, M. and Nakano, A. (2003) Rer1p, a retrieval receptor for ER membrane proteins, recognizes transmembrane domains in multiple modes. Mol. Biol. Cell 14, 3605-3616 (Pubitemid 37151612)
26. Kaether, C., Scheuermann, J., Fassler, M., Zilow, S., Shirotani, K., Valkova, C., Novak, B., Kacmar, S., Steiner, H. and Haass, C. (2007) Endoplasmic reticulum retention of the gamma-secretase complex component Pen2 by Rer1. EMBO Rep. 8, 743-748 (Pubitemid 47202453)
27. Jamain, S., Quach, H., Betancur, C., Råstam, M., Colineaux, C., Gillberg, I. C., Soderstrom, H., Giros, B., Leboyer, M., Gillberg, C. et al. (2003) Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet. 34, 27-29 (Pubitemid 36548785)
28. Tabuchi, K., Blundell, J., Etherton, M. R., Hammer, R. E., Liu, X., Powell, C. M. and Südhof, T. C. (2007) A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 318, 71-76 (Pubitemid 47538032)
29. De Jaco, A., Comoletti, D., Kovarik, Z., Gaietta, G., Radic, Z., Lockridge, O., Ellisman, M. H. and Taylor, P. (2006) A mutation linked with autism reveals a common mechanism of endoplasmic reticulum retention for the α,β-hydrolase fold protein family. J. Biol. Chem. 281, 9667-9676 (Pubitemid 43864685)
30. Scheiffele, P., Fan, J., Choih, J., Fetter, R. and Serafini, T. (2000) Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101, 657-669
31. Li, X., Serwanski, D. R., Miralles, C. P., Bahr, B. A. and De Blas, A. L. (2007) Two pools of Triton X-100-insoluble GABAA receptors are present in the brain, one associated to lipid rafts and another one to the post-synaptic GABAergic complex. J. Neurochem. 102, 1329-1345 (Pubitemid 47179808)
32. Levinson, J. N., Chéry, N., Huang, K., Wong, T. P., Gerrow, K., Kang, R., Prange, O., Wang, Y. T. and El-Husseini, A. (2005) Neuroligins mediate excitatory and inhibitory synapse formation: involvement of PSD-95 and neurexin-1β in neuroligin-induced synaptic specificity. J. Biol. Chem. 280, 17312-17319 (Pubitemid 41389200)
33. Ellgaard, L. and Helenius, A. (2003) Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4, 181-191 (Pubitemid 36288040)
34. Jacob, T. C., Moss, S. J. and Jurd, R. (2008) GABAA receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat. Rev. Neurosci. 9, 331-343 (Pubitemid 351556042)
35. Kaether, C., Haass, C. and Steiner, H. (2006) Assembly, trafficking and function of γ -secretase. Neurodegener. Dis. 3, 275-283
36. Choma, C., Gratkowski, H., Lear, J. D. and DeGrado, W. F. (2000) Asparagine-mediated self-association of a model transmembrane helix. Nat. Struct. Biol. 7, 161-166 (Pubitemid 30082515)
37. Stockner, T., Ash, W. L., MacCallum, J. L. and Tieleman, D. P. (2004) Direct simulation of transmembrane helix association: role of asparagines. Biophys. J. 87, 1650-1656 (Pubitemid 39167022)
38. Comoletti, D., De Jaco, A., Jennings, L. L., Flynn, R. E., Gaietta, G., Tsigelny, I., Ellisman, M. H. and Taylor, P. (2004) The Arg451Cys-neuroligin-3 mutation associated with autism reveals a defect in protein processing. J. Neurosci. 24, 4889-4893 (Pubitemid 38668214)
39. De Jaco, A., Lin, M. Z., Dubi, N., Comoletti, D., Miller, M. T., Camp, S., Ellisman, M., Butko, M. T., Tsien, R. Y. and Taylor, P. (2010) Neuroligin trafficking deficiencies arising from mutations in the α/β-hydrolase fold protein family. J. Biol. Chem. 285, 28674-28682