Calsyntenins Function as Synaptogenic Adhesion Molecules in Concert with Neurexins

Cell Reports

Volumn 6, Issue 6, 2014, Pages 1096-1109

  Um, Ji Won ^a   Pramanik, Gopal ^b,c   Ko, Ji Seung ^a   Song, Min Young ^d   Lee, Dongmin ^e   Kim, Hyun ^e   Park, Kang Sik ^d   Südhof, Thomas C ^f   Tabuchi, Katsuhiko ^b,c,g   Ko, Jaewon ^a  

^a Yonsei University   (South Korea)

^b SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^d Kyung Hee University Hospital   (South Korea)

^e Korea University College of Medicine   (South Korea)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA NEUREXIN; CADHERIN; CALSYNTENIN 3; CELL ADHESION MOLECULE; MESSENGER RNA; NEUREXIN; UNCLASSIFIED DRUG; CALCIUM BINDING PROTEIN; CLSTN3 PROTEIN, HUMAN; CLSTN3 PROTEIN, MOUSE; MEMBRANE PROTEIN; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; PROTEIN ALPHA NRXS; PROTEIN CST 3;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN DEVELOPMENT; BRAIN FUNCTION; CELL CULTURE; CELL DENSITY; CELL DIFFERENTIATION; CELL SIZE; CONTROLLED STUDY; EMBRYO; HIPPOCAMPUS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL; NONHUMAN; PERINATAL PERIOD; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; CYTOLOGY; FEMALE; HEK293 CELL LINE; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; PHYSIOLOGY; PREGNANCY; HIPPOCAMPAL NEURONAL CULTURE; NERVE CELL DIFFERENTIATION; NERVE FUNCTION; PRESYNAPTIC MEMBRANE; PROTEIN BINDING; PROTEIN DEPLETION; REGULATORY MECHANISM; SOMATIC CELL;

ANIMALS; CALCIUM-BINDING PROTEINS; CELL ADHESION MOLECULES, NEURONAL; CELL DIFFERENTIATION; FEMALE; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, INBRED ICR; NERVE TISSUE PROTEINS; NEURONS; PREGNANCY; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84897060360     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.02.010     Document Type: Article

References (46)

1. Araki Y., Tomita S., Yamaguchi H., Miyagi N., Sumioka A., Kirino Y., Suzuki T. Novel cadherin-related membrane proteins, Alcadeins, enhance the X11-like protein-mediated stabilization of amyloid beta-protein precursor metabolism. J.Biol. Chem. 2003, 278:49448-49458.
2. Araki Y., Kawano T., Taru H., Saito Y., Wada S., Miyamoto K., Kobayashi H., Ishikawa H.O., Ohsugi Y., Yamamoto T., et al. The novel cargo Alcadein induces vesicle association of kinesin-1 motor components and activates axonal transport. EMBO J. 2007, 26:1475-1486.
3. Arikkath J., Reichardt L.F. Cadherins and catenins at synapses: roles in synaptogenesis and synaptic plasticity. Trends Neurosci. 2008, 31:487-494.
4. Biederer T., Scheiffele P. Mixed-culture assays for analyzing neuronal synapse formation. Nat. Protoc. 2007, 2:670-676.
5. Bot N., Schweizer C., Ben Halima S., Fraering P.C. Processing of the synaptic cell adhesion molecule neurexin-3beta by Alzheimer disease alpha- and gamma-secretases. J.Biol. Chem. 2011, 286:2762-2773.
6. Calahorro F., Ruiz-Rubio M. Human alpha- and beta-NRXN1 isoforms rescue behavioral impairments of Caenorhabditis elegans neurexin-deficient mutants. Genes Brain Behav. 2013, 12:453-464.
7. Chih B., Engelman H., Scheiffele P. Control of excitatory and inhibitory synapse formation by neuroligins. Science 2005, 307:1324-1328.
8. Chubykin A.A., Atasoy D., Etherton M.R., Brose N., Kavalali E.T., Gibson J.R., Südhof T.C. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 2007, 54:919-931.
9. Craig A.M., Kang Y. Neurexin-neuroligin signaling in synapse development. Curr. Opin. Neurobiol. 2007, 17:43-52.
10. Dudanova I., Tabuchi K., Rohlmann A., Südhof T.C., Missler M. Deletion of alpha-neurexins does not cause a major impairment of axonal pathfinding or synapse formation. J.Comp. Neurol. 2007, 502:261-274.
11. Etherton M.R., Blaiss C.A., Powell C.M., Südhof T.C. Mouse neurexin-1alpha deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments. Proc. Natl. Acad. Sci. USA 2009, 106:17998-18003.
12. Gokce O., Südhof T.C. Membrane-tethered monomeric neurexin LNS-domain triggers synapse formation. J.Neurosci. 2013, 33:14617-14628.
13. Hintsch G., Zurlinden A., Meskenaite V., Steuble M., Fink-Widmer K., Kinter J., Sonderegger P. The calsyntenins-a family of postsynaptic membrane proteins with distinct neuronal expression patterns. Mol. Cell. Neurosci. 2002, 21:393-409.
14. Hoerndli F.J., Walser M., Fröhli Hoier E., de Quervain D., Papassotiropoulos A., Hajnal A. A conserved function of C. elegans CASY-1 calsyntenin in associative learning. PLoS ONE 2009, 4:e4880.
15. Hu Z., Hom S., Kudze T., Tong X.J., Choi S., Aramuni G., Zhang W., Kaplan J.M. Neurexin and neuroligin mediate retrograde synaptic inhibition in C. elegans. Science 2012, 337:980-984.
16. Hulpiau P., van Roy F. Molecular evolution of the cadherin superfamily. Int. J. Biochem. Cell Biol. 2009, 41:349-369.
17. Ikeda D.D., Duan Y., Matsuki M., Kunitomo H., Hutter H., Hedgecock E.M., Iino Y. CASY-1, an ortholog of calsyntenins/alcadeins, is essential for learning in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2008, 105:5260-5265.
18. Kang Y., Zhang X., Dobie F., Wu H., Craig A.M. Induction of GABAergic postsynaptic differentiation by alpha-neurexins. J.Biol. Chem. 2008, 283:2323-2334.
19. Ko J., Fuccillo M.V., Malenka R.C., Südhof T.C. LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron 2009, 64:791-798.
20. Ko J., Zhang C., Arac D., Boucard A.A., Brunger A.T., Südhof T.C. Neuroligin-1 performs neurexin-dependent and neurexin-independent functions in synapse validation. EMBO J. 2009, 28:3244-3255.
21. Ko J., Soler-Llavina G.J., Fuccillo M.V., Malenka R.C., Südhof T.C. Neuroligins/LRRTMs prevent activity- and Ca2+/calmodulin-dependent synapse elimination in cultured neurons. J.Cell Biol. 2011, 194:323-334.
22. Konecna A., Frischknecht R., Kinter J., Ludwig A., Steuble M., Meskenaite V., Indermühle M., Engel M., Cen C., Mateos J.M., et al. Calsyntenin-1 docks vesicular cargo to kinesin-1. Mol. Biol. Cell 2006, 17:3651-3663.
23. Krueger D.D., Tuffy L.P., Papadopoulos T., Brose N. The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses. Curr. Opin. Neurobiol. 2012, 22:412-422.
24. Maruta C., Saito Y., Hata S., Gotoh N., Suzuki T., Yamamoto T. Constitutive cleavage of the single-pass transmembrane protein alcadeinα prevents aberrant peripheral retention of Kinesin-1. PLoS ONE 2012, 7:e43058.
25. Missler M., Zhang W., Rohlmann A., Kattenstroth G., Hammer R.E., Gottmann K., Südhof T.C. Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 2003, 423:939-948.
26. Missler M., Südhof T.C., Biederer T. Synaptic cell adhesion. Cold Spring Harb. Perspect. Biol. 2012, 4:a005694.
27. Niehaus J.L., Murali M., Kauer J.A. Drugs of abuse and stress impair LTP at inhibitory synapses in the ventral tegmental area. Eur. J. Neurosci. 2010, 32:108-117.
28. Papassotiropoulos A., Stephan D.A., Huentelman M.J., Hoerndli F.J., Craig D.W., Pearson J.V., Huynh K.D., Brunner F., Corneveaux J., Osborne D., et al. Common Kibra alleles are associated with human memory performance. Science 2006, 314:475-478.
29. Pettem K.L., Yokomaku D., Luo L., Linhoff M.W., Prasad T., Connor S.A., Siddiqui T.J., Kawabe H., Chen F., Zhang L., et al. The specific α-neurexin interactor calsyntenin-3 promotes excitatory and inhibitory synapse development. Neuron 2013, 80:113-128.
30. Pettitt, J. (2005). The cadherin superfamily. WormBook 1-9.
31. Preuschhof C., Heekeren H.R., Li S.C., Sander T., Lindenberger U., Bäckman L. KIBRA and CLSTN2 polymorphisms exert interactive effects on human episodic memory. Neuropsychologia 2010, 48:402-408.
32. Ringman J.M., Schulman H., Becker C., Jones T., Bai Y., Immermann F., Cole G., Sokolow S., Gylys K., Geschwind D.H., et al. Proteomic changes in cerebrospinal fluid of presymptomatic and affected persons carrying familial Alzheimer disease mutations. Arch. Neurol. 2012, 69:96-104.
33. Scheiffele P., Fan J., Choih J., Fetter R., Serafini T. Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 2000, 101:657-669.
34. Südhof T.C. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 2008, 455:903-911.
35. Sugita S., Saito F., Tang J., Satz J., Campbell K., Südhof T.C. A stoichiometric complex of neurexins and dystroglycan in brain. J.Cell Biol. 2001, 154:435-445.
36. Suzuki T., Araki Y., Yamamoto T., Nakaya T. Trafficking of Alzheimer's disease-related membrane proteins and its participation in disease pathogenesis. J.Biochem. 2006, 139:949-955.
37. Takeichi M. The cadherin superfamily in neuronal connections and interactions. Nat. Rev. Neurosci. 2007, 8:11-20.
38. Uchida Y., Gomi F., Murayama S., Takahashi H. Calsyntenin-3 C-terminal fragment accumulates in dystrophic neurites surrounding aβ plaques in tg2576 mouse and Alzheimer disease brains: its neurotoxic role in mediating dystrophic neurite formation. Am. J. Pathol. 2013, 182:1718-1726.
39. Ullrich B., Ushkaryov Y.A., Südhof T.C. Cartography of neurexins: more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons. Neuron 1995, 14:497-507.
40. Um J.W., Ko J. LAR-RPTPs: synaptic adhesion molecules that shape synapse development. Trends Cell Biol. 2013, 23:465-475.
41. Vagnoni A., Rodriguez L., Manser C., De Vos K.J., Miller C.C. Phosphorylation of kinesin light chain 1 at serine 460 modulates binding and trafficking of calsyntenin-1. J.Cell Sci. 2011, 124:1032-1042.
42. Vagnoni A., Perkinton M.S., Gray E.H., Francis P.T., Noble W., Miller C.C. Calsyntenin-1 mediates axonal transport of the amyloid precursor protein and regulates Aβ production. Hum. Mol. Genet. 2012, 21:2845-2854.
43. Vogt L., Schrimpf S.P., Meskenaite V., Frischknecht R., Kinter J., Leone D.P., Ziegler U., Sonderegger P. Calsyntenin-1, a proteolytically processed postsynaptic membrane protein with a cytoplasmic calcium-binding domain. Mol. Cell. Neurosci. 2001, 17:151-166.
44. Yao W.D., Gainetdinov R.R., Arbuckle M.I., Sotnikova T.D., Cyr M., Beaulieu J.M., Torres G.E., Grant S.G., Caron M.G. Identification of PSD-95 as a regulator of dopamine-mediated synaptic and behavioral plasticity. Neuron 2004, 41:625-638.
45. Yim Y.S., Kwon Y., Nam J., Yoon H.I., Lee K., Kim D.G., Kim E., Kim C.H., Ko J. Slitrks control excitatory and inhibitory synapse formation with LAR receptor protein tyrosine phosphatases. Proc. Natl. Acad. Sci. USA 2013, 110:4057-4062.
46. Yin G.N., Lee H.W., Cho J.Y., Suk K. Neuronal pentraxin receptor in cerebrospinal fluid as a potential biomarker for neurodegenerative diseases. Brain Res. 2009, 1265:158-170.