39:
314:
226:, a competition hypothesis has been proposed and corroborated. This hypothesis suggests that relative levels of cadherin-catenin complexes, which are distributed amongst spines in a local area in an activity-dependent manner, determines the fate of individual spines. That is, the inter-spine competition for β-catenin determines whether a spine will be matured (increased number of complexes) or pruned (decreased number of complexes). This is a critical mechanism during the refinement of cortical circuitry that occurs throughout development.
169:
187:. Components of this complex bind to a number of different scaffolding proteins, phosphotases, kinases, and receptors. Classical cadherins have five extracellular repeating structures which bind calcium, a single transmembrane domain, and an intracellular tail with a distal cytosolic domain that binds a catenin partner. Recent work has implicated the cadherin-catenin complex in a number of different central nervous system processes such as synaptic stabilization and
544:(NMDARs) to recruit the GEF Tiam1 to the complex upon ephrinB binding. Phosphorylation of Tiam1 occurs in response to NMDAR activity, which allows for the influx of calcium that activates Tiam1. This mechanism also results in the modulation of the actin cytoskeleton. As a result of this stabilization, both EphB2 forward signaling and ephrin-B3 reverse signaling has been found to induce LTP via NMDARs.
439:
509:(ROCK), which results in the rearrangement of actin filaments. Through this mechanism, astrocytic processes are able to stabilize individual dendritic protrusions as well as their maturation into spines via ephrin/EphA signaling. Forward signaling involving the activation of EphA4 results in the stabilization of synaptic proteins at the
253:-bound nectins possess an extracellular region with three immunoglobulin-like loops. The furthest loop from the membrane is called the V-type loop and the two loops more interior are C2-type loops. Multiple nectins on one cell membrane will bind together at the V-type loop to form a cluster of nectin proteins, a process called
342:. Non-neuronal cells that artificially express neurexin are sufficient to mobilize post-synaptic specializations in co-cultured neurons; neuroligin-expressing cells are likewise able to induce markers of pre-synaptic differentiation in neighboring neurons. However, while both play an important role in synaptogenesis, these
524:
interacts with the adaptor protein glutamate-receptor-interacting protein 1 (GRIP-1) to regulate the development of excitatory dendritic shaft synapses. This process, which was identified in cultures of hippocampal neurons, revealed that Eph/ephrin B3 reverse signaling recruits GRIP1 to the membrane
148:
are the two CAM’s known to be sufficient to initiate the formation of presynaptic terminals, as addition of synCAM1 to media of co-cultured neuronal and non-neuronal cells lead to the establishment of presynaptic terminals. Homophillic binding of two synCAM1 molecules on the filopodia of axonal
414:). In addition to phosphorylating itself and neurexin, CASK promotes interactions between neurexins and actin binding proteins, thus providing a direct link by which neurexin can modulate cytoskeletal dynamics that is essential for synaptic stability and plasticity. Neurexin can also bind
202:
is widely expressed at the developing synapse and later remains near the mature active zone implicating that this complex may be well-suited to provide a link between structural changes and synaptic stability. In fact, local synaptic activity changes impact the expression of the
317:
Neurexin-neuroligin interactions promote synapse stabilization. On the presynaptic side, neurexin associates with synaptotagmin, calcium channels. On the post-synaptic side, neuroligin PDZ domain interacts with scaffolding proteins that help cluster receptor channels.
429:
upon synaptic stimulation. In this way, neurexin and neuroligin coordinate the morphological and functional aspects of the synapse which in turn permits nascent, immature contacts to stabilize into full-fledged functional platforms for neurotransmission.
406:. In the case of neurexins, their intracellular binding interactions are equally as important in recruiting the essential machinery for synaptic transmission at the active zone. Like neuroligins, neurexins possess a PDZ-domain that associates with
350:
mutant of either neurexins or neuroligins exhibit a normal number of synapses but express an embryonic lethal phenotype due to impairment of normal synaptic transmission. Therefore, they are not necessary for synapse formation
310:. The displacement of these CAMs and the formation of this junction provides the nascent synaptic membranes room to interact and mature while partitioning off the surrounding membrane and providing cytoskeletal fixation.
276:. The nectins involved in formation and stabilization of this synapse are Nectin-1 and Nectin-3 which protrude from the plasma membrane of the postsynaptic cell and presynaptic cell, respectively, forming heterophilic
525:
of the postsynaptic shaft. Once at the membrane shaft, GRIP1 helps anchor glutamate receptors below the presynaptic terminal. This process also involves the phosphorylation of a serine residue near the ephrin-B
536:
Another mechanism, found in hippocampal neurons, revealed that EphB signaling could promote spine maturation by modulating Rho GTPase activity, as observed with EphAs. Unlike EphAs, however, the
516:
Ephrin B/EphB signaling is also involved in synaptic stabilization through different mechanisms. These molecules contain cytoplasmic tails which interact with scaffolding proteins via their
204:
129:
at both pre- and postsynaptic sites and their structures consist of intracellular FERM and PDZ binding domains, a single transmembrane domain, and three extracellular
1529:
Missler M, Zhang W, Rohlmann A, Kattenstroth G, Hammer RE, Gottmann K, SĂĽdhof TC (June 2003). "Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis".
295:
As synapses mature in the CA3 region, nectins and cadherins, which affiliate closely with one another in synaptic stabilization, are shifted to the periphery of the
489:, whereas the EphA4 receptor is enriched in hippocampal neurons. This interaction, mediated by ephrin A3/EphA4 signaling, induces the recruitment and activation of
1427:
752:
Washbourne, Philip; Dityatev, Alexander; Scheiffele, Peter; Biederer, Thomas; Weiner, Joshua A.; Christopherson, Karen S.; El-Husseini, Alaa (20 October 2004).
292:. In this way, nectins form ridged connections of the cells actin architecture allowing for the synapse to develop in a controlled and stable environment.
513:. As in the EphA4/ephrinA3-mediated neuron–glia interaction, this process regulates dynamics of the actin cytoskeleton by activating ROCK through ephexin.
411:
338:. Presynaptic neurexin and its postsynaptic binding partner, neuroligin, complex early in neural development and are both known to be potent inducers of
1665:
Hata Y, Davletov B, Petrenko AG, Jahn R, SĂĽdhof TC (February 1993). "Interaction of synaptotagmin with the cytoplasmic domains of neurexins".
1851:
1592:
1510:
1403:
1105:
672:
454:
and their membrane bound ligands, the ephrins, are involved in a variety of cellular processes during development and maturation including
620:
Benson DL, Schnapp LM, Shapiro L, Huntley GW (November 2000). "Making memories stick: cell-adhesion molecules in synaptic plasticity".
359:
156:
of proteins. The cytosolic PDZ domains of synCAMs imbedded in the post-synaptic membrane interact with post-synaptic scaffold protein
1774:
32:
98:
Synaptic cell adhesion molecules (CAMs) play a crucial role in axon pathfinding and synaptic establishment between neurons during
1292:
Dean C, Dresbach T (January 2006). "Neuroligins and neurexins: linking cell adhesion, synapse formation and cognitive function".
1124:
Irie K, Shimizu K, Sakisaka T, Ikeda W, Takai Y (December 2004). "Roles and modes of action of nectins in cell-cell adhesion".
383:
334:
interactions help establish the trans-synaptic functional asymmetry essential for the stabilization and maintenance of proper
541:
358:
Beyond their extracellular contact with each other, neurexins and neuroligins also bind intracellularly to a vast network of
38:
419:
313:
125:
that promotes growth and stabilization of excitatory (not inhibitory) synapses. SynCAM’s are localized primarily in the
103:
1200:
Takai Y, Shimizu K, Ohtsuka T (October 2003). "The roles of cadherins and nectins in interneuronal synapse formation".
355:
but are essential for the maturation and integration of synapses into the functional circuits necessary for survival.
245:
and postsynaptic neuronal processes during synapse formation. There are only four well characterized nectins at the
19:
This article is about the process of synapse stabilization mediated by cell adhesion molecules. For other uses, see
595:
153:
442:
Ephrin A3/EphA4 signaling initiates a cascade of events that results in that regulation of the actin cytoskeleton.
1493:
Hortsch M (2009). "A Short
History of the Synapse – Golgi Versus Ramón y Cajal". In Hortsch M, Umemori H (eds.).
490:
265:
1790:
Bolton MM, Eroglu C (October 2009). "Look who is weaving the neural web: glial control of synapse formation".
102:
and are integral members in many synaptic processes including the correct alignment of pre- and post-synaptic
1057:"Coordinated Spine Pruning and Maturation Mediated by Inter-Spine Competition for Cadherin/Catenin Complexes"
494:
238:
180:
62:
659:. Advances in Experimental Medicine and Biology. Vol. 970. Vienna: Springer, Vienna. pp. 97–128.
257:. When two cells possessing individual cis-clusters come into contact they form a strong complex called a
73:
and the formation of the entire nervous system. In the adult nervous system, CAMs play an integral role in
510:
343:
264:
The most robust knowledge of nectin’s role in synaptic stabilization comes from the synapses made between
195:
130:
50:
28:
149:
growth cone and dendritic spine allow for initial contact between pre- and postsynaptic cell to be made.
2059:
335:
49:
is crucial in the developing and adult nervous systems and is considered a result of the late phase of
1538:
1348:
478:
168:
121:
SynCAM’s (also known as Cadm or nectin-like molecules) are a specific type of synaptic CAM found in
1616:
Zhang C, Atasoy D, Araç D, Yang X, Fucillo MV, Robison AJ, Ko J, Brunger AT, Südhof TC (May 2010).
560:
Rutishauser U, Jessell TM (July 1988). "Cell adhesion molecules in vertebrate neural development".
188:
74:
24:
1844:
Cellular
Migration and Formation of Neuronal Connections: Comprehensive Developmental Neuroscience
418:, a protein embedded in the membrane of synaptic vesicles, and can also promote associations with
366:, help localize necessary components of synaptic transmission. For example, the first neuroligin (
69:
discovered CAMs and studied their function during development, which showed CAMs are required for
1815:
1690:
1562:
1421:
1317:
1225:
459:
363:
273:
57:
through increased expression of cytoskeletal and extracellular matrix elements and postsynaptic
2036:
1985:
1936:
1884:
1847:
1807:
1770:
1742:
1682:
1647:
1598:
1588:
1554:
1506:
1475:
1409:
1399:
1376:
1309:
1274:
1217:
1182:
1141:
1101:
1078:
1034:
990:
938:
876:
832:
783:
727:
678:
668:
637:
577:
526:
300:
212:
172:
Temporal and spatial distribution of N-cadherin complexes in the developing and mature synapse
2026:
2016:
1975:
1967:
1926:
1918:
1876:
1799:
1732:
1724:
1674:
1637:
1629:
1546:
1498:
1465:
1457:
1366:
1356:
1301:
1264:
1256:
1209:
1172:
1133:
1068:
1024:
980:
972:
928:
920:
866:
822:
814:
773:
765:
717:
709:
697:
660:
629:
569:
423:
379:
307:
242:
223:
211:
leads to the dimerization of N-cadherin which is then cleaved leading the repression of CBP/
99:
58:
655:
Bukalo, Olena; Dityatev, Alexander (27 December 2012). "Synaptic Cell
Adhesion Molecules".
215:
transcription. This repression has many developmental and plasticity related implications.
475:
415:
219:
208:
137:
accumulating rapidly when axo-dendritic connections are made and helping to form a stable
1542:
1352:
2031:
2004:
1980:
1955:
1931:
1906:
1737:
1712:
1642:
1617:
1470:
1445:
1396:
Basic neurochemistry : principles of molecular, cellular, and medical neurobiology
1371:
1337:"Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter"
1336:
1269:
1244:
985:
960:
933:
908:
827:
802:
778:
753:
722:
463:
347:
339:
280:
contacts. The intracellular domain of all nectins directly bind to a protein called L-
269:
70:
66:
20:
1137:
633:
133:. During neurodevelopment, SynCAMs such as SynCAM1 act as “contact sensors” of axonal
2053:
1678:
909:"Cadherins and catenins at synapses: roles in synaptogenesis and synaptic plasticity"
455:
387:
346:
are not necessary for formation of neuronal connections during development. A triple
277:
250:
1819:
1694:
1566:
1321:
1229:
1922:
769:
467:
451:
289:
134:
115:
573:
1633:
976:
871:
854:
485:
via bi-directional ephrin/EphA signaling. Astrocytes and their processes express
1728:
1502:
1461:
713:
664:
471:
403:
296:
122:
107:
1803:
1341:
Proceedings of the
National Academy of Sciences of the United States of America
1305:
1260:
1213:
1073:
1056:
924:
438:
517:
506:
482:
426:
390:
to the proper post-synaptic locale. Similarly, another isoform of neuroligin (
371:
331:
304:
299:
and form the puncta adherens junction (PAJ). The PAJ functions much like the
145:
111:
1602:
1413:
261:
which provides adhesion and, in some cases, signaling between the two cells.
1880:
1361:
521:
486:
1989:
1811:
1746:
1651:
1558:
1479:
1380:
1313:
1278:
1221:
1186:
1145:
1082:
1038:
994:
942:
880:
836:
787:
731:
682:
641:
2040:
2021:
1940:
1888:
1686:
581:
395:
327:
176:
138:
78:
54:
1971:
1550:
801:
Dalva, Matthew; McClelland, Andrew; Kayser, Matthew (14 February 2007).
198:
exhibit distinct spatial and temporal expression patterns. For example,
1618:"Neurexins physically and functionally interact with GABA(A) receptors"
1177:
1160:
529:(proximal to the PDZ-binding motif) that leads to the stabilization of
246:
184:
1846:. San Diego, CA: Elsevier Science & Technology. pp. 659–669.
498:
497:(GEF), ephexin1. Phosphorylated ephexin1 can then activate the small
447:
402:, and is responsible for activation of the synaptic adapator protein
234:
157:
82:
2005:"DC-determined displacement of the nystagmus beat in rotatory tests"
1029:
1012:
818:
65:(CAMs) play a large role in synaptic maintenance and stabilization.
53:(LTP). The mechanism involves strengthening and maintaining active
537:
437:
391:
375:
367:
312:
285:
281:
167:
126:
37:
1867:
Flannery DB (September 1988). "Nondisjunction in Down syndrome".
530:
502:
407:
399:
199:
160:
which helps anchor the complex to the underlying cytoskeleton.
1161:"The role of nectins in different types of cell-cell adhesion"
961:"Cadherins and catenins in dendrite and synapse morphogenesis"
803:"Cell adhesion molecules: signalling functions at the synapse"
114:, integration of postsynaptic receptors and anchoring to the
520:
domains to stabilize newly formed CNS synapses. For example,
696:
Biederer, Thomas; Missler, Markus; SĂĽdhof, Thomas (2012).
540:
receptor has been shown to interact with the postsynaptic
855:"Cadherins: actin with the cytoskeleton to form synapses"
1711:
Lisabeth EM, Falivelli G, Pasquale EB (September 2013).
288:
binding protein that binds to the F-actin of the actin
16:
Modifying synaptic strength via cell adhesion molecules
1245:"Neurexin-neuroligin signaling in synapse development"
1013:"Neural development: a complex competition for spines"
362:
and scaffolding structures, which in concert with the
241:. These CAMs are involved in the initial contact of
183:
that form complexes with cytosolic partners known as
2003:
Lundgren A, Tibbling L, Henriksson NG (March 2018).
1055:
Bian WJ, Miao WY, He SJ, Qiu Z, Yu X (August 2015).
505:, leading to subsequent activation of its effector,
1769:. New York, NY: Garland Science. pp. 299–302.
708:(4). Cold Spring Harbor Laboratory Press: a005694.
207:complexes. An increase in activity at a particular
1394:Brady ST, Siegel GJ, Albers RW, Price DL (2012).
42:Synaptic stabilization by cell adhesion molecules
446:Non-traditional adhesion molecules, such as the
1524:
1522:
1444:Missler M, SĂĽdhof TC, Biederer T (April 2012).
1439:
1437:
1006:
1004:
902:
900:
898:
896:
894:
892:
890:
61:, while pruning less active ones. For example,
1907:"Viral myocarditis as an incidental discovery"
1578:
1576:
754:"Cell Adhesion Molecules in Synapse Formation"
1837:
1835:
1833:
1831:
1829:
1159:Rikitake Y, Mandai K, Takai Y (August 2012).
954:
952:
8:
1126:Seminars in Cell & Developmental Biology
1119:
1117:
1050:
1048:
848:
846:
118:to ensure stability of synaptic components.
1398:(Eighth ed.). Waltham, Massachusetts.
907:Arikkath J, Reichardt LF (September 2008).
412:Calcium-calmodulin-dependent protein kinase
1760:
1758:
1756:
1717:Cold Spring Harbor Perspectives in Biology
1706:
1704:
1450:Cold Spring Harbor Perspectives in Biology
1426:: CS1 maint: location missing publisher (
959:Seong E, Yuan L, Arikkath J (April 2015).
702:Cold Spring Harbor Perspectives in Biology
2030:
2020:
1979:
1930:
1736:
1641:
1469:
1370:
1360:
1268:
1176:
1072:
1028:
984:
932:
870:
826:
777:
721:
450:, also help stabilize synaptic contacts.
1497:. Springer, New York, NY. pp. 1–9.
422:which mediate the ion flux required for
1900:
1898:
552:
1419:
493:(Cdk5), which then phosphorylates the
249:, they are Nectin-1, 2, 3, and 4. All
1954:Arvanitis D, Davy A (February 2008).
7:
1869:American Journal of Medical Genetics
1713:"Eph receptor signaling and ephrins"
398:, a scaffolding protein specific to
106:, vesicular recycling in regards to
370:) discovered was identified by its
179:are calcium- dependent, homophilic
1243:Craig AM, Kang Y (February 2007).
14:
1098:Development of the Nervous System
33:Development of the nervous system
2009:Practica Oto-Rhino-Laryngologica
1956:"Eph/ephrin signaling: networks"
1792:Current Opinion in Neurobiology
1249:Current Opinion in Neurobiology
1202:Current Opinion in Neurobiology
1923:10.1016/j.brainres.2006.11.033
770:10.1523/JNEUROSCI.3339-04.2004
542:N-methyl-D-aspartate receptors
1:
1587:. Amsterdam: Academic Press.
1335:Nam CI, Chen L (April 2005).
1138:10.1016/s1084-9521(04)00088-6
965:Cell Adhesion & Migration
634:10.1016/S0962-8924(00)01838-9
596:"Gerald M. Edelman biography"
574:10.1152/physrev.1988.68.3.819
420:voltage-gated calcium channel
274:CA3 region of the hippocampus
1679:10.1016/0896-6273(93)90320-Q
1634:10.1016/j.neuron.2010.04.008
1585:Encyclopedia of neuroscience
1096:Sanes D (January 25, 2011).
1017:Nature Reviews. Neuroscience
977:10.4161/19336918.2014.994919
872:10.1016/j.neuron.2005.06.024
104:signal transduction pathways
1729:10.1101/cshperspect.a009159
1503:10.1007/978-0-387-92708-4_1
1462:10.1101/cshperspect.a005694
714:10.1101/cshperspect.a005694
665:10.1007/978-3-7091-0932-8_5
2076:
1905:Lerner AM (October 1990).
1804:10.1016/j.conb.2009.09.007
1767:Developmental Neurobiology
1306:10.1016/j.tins.2005.11.003
1261:10.1016/j.conb.2007.01.011
1214:10.1016/j.conb.2003.09.003
1100:(3rd ed.). Elsevier.
1074:10.1016/j.cell.2015.07.018
1011:Whalley K (October 2015).
925:10.1016/j.tins.2008.07.001
18:
1842:Rubenstein J (May 2013).
491:cyclin-dependent kinase 5
237:are a distinct family of
1446:"Synaptic cell adhesion"
698:"Synaptic Cell Adhesion"
386:that functionally links
1960:Genes & Development
1881:10.1002/ajmg.1320310123
1362:10.1073/pnas.0502038102
1294:Trends in Neurosciences
1165:Journal of Cell Science
913:Trends in Neurosciences
758:Journal of Neuroscience
533:receptors at synapses.
495:guanine exchange factor
239:cell adhesion molecules
181:cell adhesion molecules
63:cell adhesion molecules
853:Bamji SX (July 2005).
622:Trends in Cell Biology
511:neuromuscular junction
443:
384:glutamatergic synapses
344:cell adhesion molecule
319:
196:central nervous system
194:Many cadherins in the
173:
152:synCAMs belong to the
51:long-term potentiation
47:Synaptic stabilization
43:
29:Cell adhesion molecule
2022:10.3892/etm.2018.5702
562:Physiological Reviews
441:
336:synaptic transmission
316:
171:
41:
481:may be regulated by
434:Ephrin-Eph signaling
1972:10.1101/gad.1630408
1917:(10): 81–4, 87–90.
1551:10.1038/nature01755
1543:2003Natur.423..939M
1353:2005PNAS..102.6137N
657:Synaptic Plasticity
400:GABA-ergic synapses
323:Neurexin-neuroligin
144:synCAM1 along with
75:synaptic plasticity
25:Synaptic plasticity
1765:Bianchi L (2018).
1583:Squire LR (2009).
1495:The Sticky Synapse
1178:10.1242/jcs.099572
1171:(Pt 16): 3713–22.
460:neuronal migration
444:
364:actin cytoskeleton
320:
301:adherens junctions
284:. L-Afadin is an
174:
44:
1911:Hospital Practice
1853:978-0-12-397266-8
1594:978-0-08-096393-8
1512:978-0-387-92707-7
1405:978-0-12-374947-5
1107:978-0-08-092320-8
764:(42): 9244–9249.
674:978-3-7091-0932-8
527:carboxyl terminus
394:) interacts with
378:, a well-known a
272:dendrites in the
259:trans-interaction
59:scaffold proteins
2067:
2045:
2044:
2034:
2024:
2000:
1994:
1993:
1983:
1951:
1945:
1944:
1934:
1902:
1893:
1892:
1864:
1858:
1857:
1839:
1824:
1823:
1787:
1781:
1780:
1762:
1751:
1750:
1740:
1708:
1699:
1698:
1662:
1656:
1655:
1645:
1613:
1607:
1606:
1580:
1571:
1570:
1537:(6943): 939–48.
1526:
1517:
1516:
1490:
1484:
1483:
1473:
1441:
1432:
1431:
1425:
1417:
1391:
1385:
1384:
1374:
1364:
1332:
1326:
1325:
1289:
1283:
1282:
1272:
1240:
1234:
1233:
1197:
1191:
1190:
1180:
1156:
1150:
1149:
1121:
1112:
1111:
1093:
1087:
1086:
1076:
1052:
1043:
1042:
1032:
1008:
999:
998:
988:
956:
947:
946:
936:
904:
885:
884:
874:
850:
841:
840:
830:
798:
792:
791:
781:
749:
743:
742:
740:
738:
725:
693:
687:
686:
652:
646:
645:
617:
611:
610:
608:
606:
592:
586:
585:
557:
424:neurotransmitter
380:scaffold protein
360:adaptor proteins
205:cadherin-catenin
164:Cadherin-catenin
100:neurodevelopment
2075:
2074:
2070:
2069:
2068:
2066:
2065:
2064:
2050:
2049:
2048:
2002:
2001:
1997:
1953:
1952:
1948:
1904:
1903:
1896:
1866:
1865:
1861:
1854:
1841:
1840:
1827:
1789:
1788:
1784:
1777:
1764:
1763:
1754:
1710:
1709:
1702:
1664:
1663:
1659:
1615:
1614:
1610:
1595:
1582:
1581:
1574:
1528:
1527:
1520:
1513:
1492:
1491:
1487:
1443:
1442:
1435:
1418:
1406:
1393:
1392:
1388:
1347:(17): 6137–42.
1334:
1333:
1329:
1291:
1290:
1286:
1242:
1241:
1237:
1199:
1198:
1194:
1158:
1157:
1153:
1123:
1122:
1115:
1108:
1095:
1094:
1090:
1054:
1053:
1046:
1030:10.1038/nrn4024
1010:
1009:
1002:
958:
957:
950:
906:
905:
888:
852:
851:
844:
819:10.1038/nrn2075
800:
799:
795:
751:
750:
746:
736:
734:
695:
694:
690:
675:
654:
653:
649:
619:
618:
614:
604:
602:
594:
593:
589:
559:
558:
554:
550:
476:dendritic spine
436:
374:which binds to
325:
232:
220:dendritic spine
218:In the case of
166:
96:
91:
36:
17:
12:
11:
5:
2073:
2071:
2063:
2062:
2052:
2051:
2047:
2046:
1995:
1946:
1894:
1859:
1852:
1825:
1782:
1775:
1752:
1723:(9): a009159.
1700:
1657:
1608:
1593:
1572:
1518:
1511:
1485:
1456:(4): a005694.
1433:
1404:
1386:
1327:
1284:
1235:
1192:
1151:
1113:
1106:
1088:
1044:
1000:
948:
886:
842:
813:(3): 206–220.
793:
744:
688:
673:
647:
628:(11): 473–82.
612:
600:Nobelprize.org
587:
551:
549:
546:
464:synaptogenesis
435:
432:
388:NMDA receptors
348:knockout mouse
340:synaptogenesis
324:
321:
270:pyramidal cell
268:terminals and
255:cis-clustering
231:
228:
222:formation and
165:
162:
154:Ig superfamily
95:
92:
90:
87:
71:cell migration
67:Gerald Edelman
21:Synaptogenesis
15:
13:
10:
9:
6:
4:
3:
2:
2072:
2061:
2058:
2057:
2055:
2042:
2038:
2033:
2028:
2023:
2018:
2014:
2010:
2006:
1999:
1996:
1991:
1987:
1982:
1977:
1973:
1969:
1966:(4): 416–29.
1965:
1961:
1957:
1950:
1947:
1942:
1938:
1933:
1928:
1924:
1920:
1916:
1912:
1908:
1901:
1899:
1895:
1890:
1886:
1882:
1878:
1874:
1870:
1863:
1860:
1855:
1849:
1845:
1838:
1836:
1834:
1832:
1830:
1826:
1821:
1817:
1813:
1809:
1805:
1801:
1797:
1793:
1786:
1783:
1778:
1776:9780815344827
1772:
1768:
1761:
1759:
1757:
1753:
1748:
1744:
1739:
1734:
1730:
1726:
1722:
1718:
1714:
1707:
1705:
1701:
1696:
1692:
1688:
1684:
1680:
1676:
1673:(2): 307–15.
1672:
1668:
1661:
1658:
1653:
1649:
1644:
1639:
1635:
1631:
1628:(3): 403–16.
1627:
1623:
1619:
1612:
1609:
1604:
1600:
1596:
1590:
1586:
1579:
1577:
1573:
1568:
1564:
1560:
1556:
1552:
1548:
1544:
1540:
1536:
1532:
1525:
1523:
1519:
1514:
1508:
1504:
1500:
1496:
1489:
1486:
1481:
1477:
1472:
1467:
1463:
1459:
1455:
1451:
1447:
1440:
1438:
1434:
1429:
1423:
1415:
1411:
1407:
1401:
1397:
1390:
1387:
1382:
1378:
1373:
1368:
1363:
1358:
1354:
1350:
1346:
1342:
1338:
1331:
1328:
1323:
1319:
1315:
1311:
1307:
1303:
1299:
1295:
1288:
1285:
1280:
1276:
1271:
1266:
1262:
1258:
1254:
1250:
1246:
1239:
1236:
1231:
1227:
1223:
1219:
1215:
1211:
1207:
1203:
1196:
1193:
1188:
1184:
1179:
1174:
1170:
1166:
1162:
1155:
1152:
1147:
1143:
1139:
1135:
1132:(6): 643–56.
1131:
1127:
1120:
1118:
1114:
1109:
1103:
1099:
1092:
1089:
1084:
1080:
1075:
1070:
1067:(4): 808–22.
1066:
1062:
1058:
1051:
1049:
1045:
1040:
1036:
1031:
1026:
1022:
1018:
1014:
1007:
1005:
1001:
996:
992:
987:
982:
978:
974:
971:(3): 202–13.
970:
966:
962:
955:
953:
949:
944:
940:
935:
930:
926:
922:
919:(9): 487–94.
918:
914:
910:
903:
901:
899:
897:
895:
893:
891:
887:
882:
878:
873:
868:
864:
860:
856:
849:
847:
843:
838:
834:
829:
824:
820:
816:
812:
808:
804:
797:
794:
789:
785:
780:
775:
771:
767:
763:
759:
755:
748:
745:
733:
729:
724:
719:
715:
711:
707:
703:
699:
692:
689:
684:
680:
676:
670:
666:
662:
658:
651:
648:
643:
639:
635:
631:
627:
623:
616:
613:
601:
597:
591:
588:
583:
579:
575:
571:
568:(3): 819–57.
567:
563:
556:
553:
547:
545:
543:
539:
534:
532:
528:
523:
519:
514:
512:
508:
504:
500:
496:
492:
488:
484:
480:
477:
473:
469:
465:
461:
457:
456:axon guidance
453:
452:Eph receptors
449:
440:
433:
431:
428:
425:
421:
417:
416:synaptotagmin
413:
409:
405:
401:
397:
393:
389:
385:
381:
377:
373:
369:
365:
361:
356:
354:
349:
345:
341:
337:
333:
329:
322:
315:
311:
309:
306:
302:
298:
293:
291:
287:
283:
279:
278:extracellular
275:
271:
267:
262:
260:
256:
252:
248:
244:
240:
236:
229:
227:
225:
221:
216:
214:
210:
206:
201:
197:
192:
190:
186:
182:
178:
170:
163:
161:
159:
155:
150:
147:
142:
140:
136:
132:
128:
124:
119:
117:
113:
109:
105:
101:
93:
89:Types of CAMs
88:
86:
84:
80:
76:
72:
68:
64:
60:
56:
52:
48:
40:
34:
30:
26:
22:
2060:Neuroscience
2015:(1): 54–64.
2012:
2008:
1998:
1963:
1959:
1949:
1914:
1910:
1875:(1): 181–2.
1872:
1868:
1862:
1843:
1798:(5): 491–7.
1795:
1791:
1785:
1766:
1720:
1716:
1670:
1666:
1660:
1625:
1621:
1611:
1584:
1534:
1530:
1494:
1488:
1453:
1449:
1395:
1389:
1344:
1340:
1330:
1297:
1293:
1287:
1255:(1): 43–52.
1252:
1248:
1238:
1208:(5): 520–6.
1205:
1201:
1195:
1168:
1164:
1154:
1129:
1125:
1097:
1091:
1064:
1060:
1020:
1016:
968:
964:
916:
912:
865:(2): 175–8.
862:
858:
810:
806:
796:
761:
757:
747:
735:. Retrieved
705:
701:
691:
656:
650:
625:
621:
615:
603:. Retrieved
599:
590:
565:
561:
555:
535:
515:
468:axon pruning
445:
357:
352:
326:
294:
290:cytoskeleton
263:
258:
254:
233:
217:
193:
175:
151:
143:
135:growth cones
120:
116:cytoskeleton
97:
77:relating to
46:
45:
1300:(1): 21–9.
1023:(10): 577.
472:hippocampus
404:collybistin
297:active zone
266:mossy fiber
243:presynaptic
123:vertebrates
108:endocytosis
548:References
507:Rho-kinase
483:astrocytes
479:morphology
427:exocytosis
372:PDZ domain
332:Neuroligin
305:epithelial
200:N-cadherin
189:plasticity
146:neuroligin
131:Ig-domains
112:exocytosis
1603:503584095
1422:cite book
1414:754167839
522:Ephrin B3
487:ephrin A3
470:. In the
177:Cadherins
141:complex.
2054:Category
1990:18281458
1820:44625935
1812:19879129
1747:24003208
1695:12954601
1652:20471353
1567:10315093
1559:12827191
1480:22278667
1381:15837930
1322:11664697
1314:16337696
1279:17275284
1230:10053035
1222:14630213
1187:23027581
1146:15561584
1083:26255771
1039:26307326
995:25914083
943:18684518
881:16039559
837:17299456
788:15496659
737:12 March
732:22278667
683:22351053
642:11050419
605:13 March
396:gephyrin
328:Neurexin
251:membrane
185:catenins
139:adhesion
79:learning
55:synapses
2041:5795627
2032:5795627
1981:2731651
1941:2170431
1932:2170431
1889:2975924
1738:3753714
1687:8439414
1643:3243752
1539:Bibcode
1471:3312681
1372:1087954
1349:Bibcode
1270:2820508
986:4594442
934:2623250
828:4756920
779:6730099
723:3312681
582:3293093
448:ephrins
308:tissues
247:synapse
235:Nectins
224:pruning
94:SynCAMs
2039:
2029:
1988:
1978:
1939:
1929:
1887:
1850:
1818:
1810:
1773:
1745:
1735:
1693:
1685:
1667:Neuron
1650:
1640:
1622:Neuron
1601:
1591:
1565:
1557:
1531:Nature
1509:
1478:
1468:
1412:
1402:
1379:
1369:
1320:
1312:
1277:
1267:
1228:
1220:
1185:
1144:
1104:
1081:
1037:
993:
983:
941:
931:
879:
859:Neuron
835:
825:
807:Nature
786:
776:
730:
720:
681:
671:
640:
580:
499:GTPase
466:, and
353:per se
282:Afadin
230:Nectin
158:PSD-95
83:memory
31:, and
1816:S2CID
1691:S2CID
1563:S2CID
1318:S2CID
1226:S2CID
538:EphB2
392:NLGN2
376:PSD95
368:NLGN1
286:actin
209:spine
127:brain
2037:PMID
1986:PMID
1937:PMID
1885:PMID
1848:ISBN
1808:PMID
1771:ISBN
1743:PMID
1683:PMID
1648:PMID
1599:OCLC
1589:ISBN
1555:PMID
1507:ISBN
1476:PMID
1428:link
1410:OCLC
1400:ISBN
1377:PMID
1310:PMID
1275:PMID
1218:PMID
1183:PMID
1142:PMID
1102:ISBN
1079:PMID
1061:Cell
1035:PMID
991:PMID
939:PMID
877:PMID
833:PMID
784:PMID
739:2018
728:PMID
679:PMID
669:ISBN
638:PMID
607:2018
578:PMID
531:AMPA
503:RhoA
408:CASK
213:CREB
110:and
81:and
2027:PMC
2017:doi
1976:PMC
1968:doi
1927:PMC
1919:doi
1877:doi
1800:doi
1733:PMC
1725:doi
1675:doi
1638:PMC
1630:doi
1547:doi
1535:423
1499:doi
1466:PMC
1458:doi
1367:PMC
1357:doi
1345:102
1302:doi
1265:PMC
1257:doi
1210:doi
1173:doi
1169:125
1134:doi
1069:doi
1065:162
1025:doi
981:PMC
973:doi
929:PMC
921:doi
867:doi
823:PMC
815:doi
774:PMC
766:doi
718:PMC
710:doi
661:doi
630:doi
570:doi
518:PDZ
382:at
303:in
2056::
2035:.
2025:.
2013:31
2011:.
2007:.
1984:.
1974:.
1964:22
1962:.
1958:.
1935:.
1925:.
1915:25
1913:.
1909:.
1897:^
1883:.
1873:31
1871:.
1828:^
1814:.
1806:.
1796:19
1794:.
1755:^
1741:.
1731:.
1719:.
1715:.
1703:^
1689:.
1681:.
1671:10
1669:.
1646:.
1636:.
1626:66
1624:.
1620:.
1597:.
1575:^
1561:.
1553:.
1545:.
1533:.
1521:^
1505:.
1474:.
1464:.
1452:.
1448:.
1436:^
1424:}}
1420:{{
1408:.
1375:.
1365:.
1355:.
1343:.
1339:.
1316:.
1308:.
1298:29
1296:.
1273:.
1263:.
1253:17
1251:.
1247:.
1224:.
1216:.
1206:13
1204:.
1181:.
1167:.
1163:.
1140:.
1130:15
1128:.
1116:^
1077:.
1063:.
1059:.
1047:^
1033:.
1021:16
1019:.
1015:.
1003:^
989:.
979:.
967:.
963:.
951:^
937:.
927:.
917:31
915:.
911:.
889:^
875:.
863:47
861:.
857:.
845:^
831:.
821:.
809:.
805:.
782:.
772:.
762:24
760:.
756:.
726:.
716:.
704:.
700:.
677:.
667:.
636:.
626:10
624:.
598:.
576:.
566:68
564:.
501:,
474:,
462:,
458:,
191:.
85:.
27:,
23:,
2043:.
2019::
1992:.
1970::
1943:.
1921::
1891:.
1879::
1856:.
1822:.
1802::
1779:.
1749:.
1727::
1721:5
1697:.
1677::
1654:.
1632::
1605:.
1569:.
1549::
1541::
1515:.
1501::
1482:.
1460::
1454:4
1430:)
1416:.
1383:.
1359::
1351::
1324:.
1304::
1281:.
1259::
1232:.
1212::
1189:.
1175::
1148:.
1136::
1110:.
1085:.
1071::
1041:.
1027::
997:.
975::
969:9
945:.
923::
883:.
869::
839:.
817::
811:8
790:.
768::
741:.
712::
706:4
685:.
663::
644:.
632::
609:.
584:.
572::
410:(
330:-
35:.
Text is available under the Creative Commons Attribution-ShareAlike License. Additional terms may apply.