Zebrafish calsyntenins mediate homophilic adhesion through their amino-terminal cadherin repeats

Neuroscience

Volumn 286, Issue , 2015, Pages 87-96

  Ortiz Medina, H ^a   Emond, M R ^a   Jontes, J D ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Adhesion; Cadherin; Calsyntenin; Zebrafish

Indexed keywords

CADHERIN; CALSYNTENINS PROTEIN; UNCLASSIFIED DRUG; ZEBRAFISH PROTEIN;

ADULT; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CLSTN1 GENE; CLSTN2 GENE; CLSTN3 GENE; CONTROLLED STUDY; EMBRYO; GENE; GENE EXPRESSION; MOLECULAR CLONING; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; STRUCTURE ACTIVITY RELATION; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; BRAIN; CELL ADHESION; EMBRYOLOGY; GENETICS; METABOLISM;

ANIMALS; BRAIN; CADHERINS; CELL ADHESION; EMBRYO, NONMAMMALIAN; GENE EXPRESSION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84916603963     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.11.030     Document Type: Article

References (43)

1. Araki Y., Kawano T., Taru H., Saito Y., Wada S., Miyamoto K., Kobayashi H., Ishikawa H.O., Ohsugi Y., Yamamoto T., Matsuno K., Kinjo M., Suzuki T. The novel cargo Alcadein induces vesicle association of kinesin-1 motor components and activates axonal transport. EMBO J 2007, 26:1475-1486.
2. Araki Y., Miyagi N., Kato N., Yoshida T., Wada S., Nishimura M., Komano H., Yamamoto T., De Strooper B., Yamamoto K., Suzuki T. Coordinated metabolism of Alcadein and amyloid beta-protein precursor regulates FE65-dependent gene transactivation. J Biol Chem 2004, 279:24343-24354.
3. 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.
4. Biswas S., Emond M.R., Jontes J.D. Protocadherin-19 and N-cadherin interact to control cell movements during anterior neurulation. J Cell Biol 2010, 191:1029-1041.
5. Blevins C.J., Emond M.R., Biswas S., Jontes J.D. Differential expression, alternative splicing, and adhesive properties of the zebrafish delta1-protocadherins. Neuroscience 2011, 199:523-534.
6. Boggon T.J., Murray J., Chappuis-Flament S., Wong E., Gumbiner B.M., Shapiro L. C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 2002, 296:1308-1313.
7. Chen X., Gumbiner B.M. Paraxial protocadherin mediates cell sorting and tissue morphogenesis by regulating C-cadherin adhesion activity. J Cell Biol 2006, 174:301-313.
8. Crawley S.W., Shifrin D.A., Grega-Larson N.E., McConnell R.E., Benesh A.E., Mao S., Zheng Y., Zheng Q.Y., Nam K.T., Millis B.A., Kachar B., Tyska M.J. Intestinal brush border assembly driven by protocadherin-based intermicrovillar adhesion. Cell 2014, 157:433-446.
9. Emond M.R., Biswas S., Blevins C.J., Jontes J.D. A complex of Protocadherin-19 and N-cadherin mediates a novel mechanism of cell adhesion. J Cell Biol 2011, 195:1115-1121.
10. Emond M.R., Jontes J.D. Bead aggregation assays for the characterization of putative cell adhesion molecules. J Vis Exp 2014, 10.3791/51762.
11. Hatta K., Nose A., Nagafuchi A., Takeichi M. Cloning and expression of cDNA encoding a neural calcium-dependent cell adhesion molecule: its identity in the cadherin gene family. J Cell Biol 1988, 106:873-881.
12. 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.
13. Hoerndli F.J., Walser M., Frohli 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.
14. 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. PNAS 2008, 105:5260-5265.
15. Ishiuchi T., Misaki K., Yonemura S., Takeichi M., Tanoue T. Mammalian Fat and Dachsous cadherins regulate apical membrane organization in the embryonic cerebral cortex. J Cell Biol 2009, 185:959-967.
16. Jacobsen L.K., Picciotto M.R., Heath C.J., Mencl W.E., Gelernter J. Allelic variation of calsyntenin 2 (CLSTN2) modulates the impact of developmental tobacco smoke exposure on mnemonic processing in adolescents. Biol Psychiatry 2009, 65:671-679.
17. Jin X., Walker M.A., Felsovalyi K., Vendome J., Bahna F., Mannepalli S., Cosmanescu F., Ahlsen G., Honig B., Shapiro L. Crystal structures of Drosophila N-cadherin ectodomain regions reveal a widely used class of Ca(2)+-free interdomain linkers. PNAS 2012, 109:E127-E134.
18. Kazmierczak P., Sakaguchi H., Tokita J., Wilson-Kubalek E.M., Milligan R.A., Muller U., Kachar B. Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells. Nature 2007, 449:87-91.
19. Konecna A., Frischknecht R., Kinter J., Ludwig A., Steuble M., Meskenaite V., Indermuhle M., Engel M., Cen C., Mateos J.M., Streit P., Sonderegger P. Calsyntenin-1 docks vesicular cargo to kinesin-1. Mol Biol Cell 2006, 17:3651-3663.
20. Ludwig A., Blume J., Diep T.M., Yuan J., Mateos J.M., Leuthauser K., Steuble M., Streit P., Sonderegger P. Calsyntenins mediate TGN exit of APP in a kinesin-1-dependent manner. Traffic 2009, 10:572-589.
21. Maruta C., Saito Y., Hata S., Gotoh N., Suzuki T., Yamamoto T. Constitutive cleavage of the single-pass transmembrane protein alcadeinalpha prevents aberrant peripheral retention of Kinesin-1. PloS One 2012, 7:e43058.
22. Mizumaru C., Saito Y., Ishikawa T., Yoshida T., Yamamoto T., Nakaya T., Suzuki T. Suppression of APP-containing vesicle trafficking and production of beta-amyloid by AID/DHHC-12 protein. J Neurochem 2009, 111:1213-1224.
23. Morishita H., Umitsu M., Murata Y., Shibata N., Udaka K., Higuchi Y., Akutsu H., Yamaguchi T., Yagi T., Ikegami T. Structure of the cadherin-related neuronal receptor/protocadherin-alpha first extracellular cadherin domain reveals diversity across cadherin families. J Biol Chem 2006, 281:33650-33663.
24. Nollet F., Kools P., van Roy F. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 2000, 299:551-572.
25. Nose A., Nagafuchi A., Takeichi M. Expressed recombinant cadherins mediate cell sorting in model systems. Cell 1988, 54:993-1001.
26. Ohno H., Kato S., Naito Y., Kunitomo H., Tomioka M., Iino Y. Role of synaptic phosphatidylinositol 3-kinase in a behavioral learning response in C. elegans. Science 2014, 345:313-317.
27. Pettem K.L., Yokomaku D., Luo L., Linhoff M.W., Prasad T., Connor S.A., Siddiqui T.J., Kawabe H., Chen F., Zhang L., Rudenko G., Wang Y.T., Brose N., Craig A.M. The specific alpha-neurexin interactor calsyntenin-3 promotes excitatory and inhibitory synapse development. Neuron 2013, 80:113-128.
28. Ponomareva O.Y., Holmen I.C., Sperry A.J., Eliceiri K.W., Halloran M.C. Calsyntenin-1 regulates axon branching and endosomal trafficking during sensory neuron development in vivo. J Neurosci 2014, 34:9235-9248.
29. Preuschhof C., Heekeren H.R., Li S.C., Sander T., Lindenberger U., Backman L. KIBRA and CLSTN2 polymorphisms exert interactive effects on human episodic memory. Neuropsychologia 2010, 48:402-408.
30. Redies C. Cadherins in the central nervous system. Prog Neurobiol 2000, 61:611-648.
31. Sivasankar S., Zhang Y., Nelson W.J., Chu S. Characterizing the initial encounter complex in cadherin adhesion. Structure 2009, 17:1075-1081.
32. Sotomayor M., Weihofen W.A., Gaudet R., Corey D.P. Structure of a force-conveying cadherin bond essential for inner-ear mechanotransduction. Nature 2012, 492:128-132.
33. Ster J., Steuble M., Orlando C., Diep T.M., Akhmedov A., Raineteau O., Pernet V., Sonderegger P., Gerber U. Calsyntenin-1 regulates targeting of dendritic NMDA receptors and dendritic spine maturation in CA1 hippocampal pyramidal cells during postnatal development. J Neurosci 2014, 34:8716-8727.
34. 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.
35. Takeichi M. Functional correlation between cell adhesive properties and some cell surface proteins. J Cell Biol 1977, 75:464-474.
36. Takeichi M. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 1988, 102:639-655.
37. Takeichi M. Cadherins: a molecular family important in selective cell-cell adhesion. Annu Rev Biochem 1990, 59:237-252.
38. Um J.W., Pramanik G., Ko J.S., Song M.Y., Lee D., Kim H., Park K.S., Sudhof T.C., Tabuchi K., Ko J. Calsyntenins function as synaptogenic adhesion molecules in concert with neurexins. Cell Rep 2014, 6:1096-1109.
39. 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 Abeta production. Hum Mol Genet 2012, 21:2845-2854.
40. Vendome J., Posy S., Jin X., Bahna F., Ahlsen G., Shapiro L., Honig B. Molecular design principles underlying beta-strand swapping in the adhesive dimerization of cadherins. Nat Struct Mol Biol 2011, 18:693-700.
41. 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.
42. Westerfield M. The zebrafish book 1995, University of Oregon Press, Eugene, OR.
43. Zhang H., Kranzler H.R., Poling J., Gruen J.R., Gelernter J. Cognitive flexibility is associated with KIBRA variant and modulated by recent tobacco use. Neuropsychopharmacology 2009, 34:2508-2516.