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Adhesion Junctions Associated with Synapses and Dendritic Spines

by Josef Spacek

A chemical synapse is a modified intercellular junction specialized for signaling between neurons. However, a great number of spinous synapses (at least 77% of perforated synapses) are inhomogeneous and contain an undifferentiated vesicle-free portion having the characteristics of punctum adherens junctions (Fig 1). Recent immunocytochemical studies have shown that adhesion molecules, such as cadherins, catenins, and neural cell adhesion molecules (NCAMs) are concentrated in these areas. These molecules are important for differentiation of neural tissue and synaptic plasticity.

Fig. 1: The hippocampal perforated spine synapse as it would look under the classical view of homogeneous synaptic ultrastructure (A). In reality the synaptic ultrastructure is inhomogeneous (B), containing vesicle-free adherent puncta (yellow), vesicle-free transitional zones (blue) and vesicle-associated synaptic active zone (red). See Spacek and Harris (1998) for details.

We found an intimate relationship between the spine apparatus and the synapse-associating punctum adherens: a granulofilamentous material radiates from the inner dense plates of the spine apparatus into the punctum. Our suggestion is that the spine apparatus can synthesize proteins to extend the synapse (Fig. 2).

Fig. 2: Our model of how the synapse can enlarge during synaptic plasticity. (Ax) axon terminal; (DS) dendritic spine; (SA) spine apparatus; (yellow) material of the inner dense plate; (PA; yellow) punctum adherens; (SAZ, red) the extending synaptic active zone.

In addition to the punctum adherens accompanying the synapse, numerous dendritic spines, especially those of mushroom-shaped type with a perforated synapse, possess another punctum adherens fixing an astrocytic process to the spine (Fig. 3). The astrocytes play an important role in maintainance of ionic and neurotransmitter concentrations in the vicinity of the synapse (Ventura and Harris, 1999).

Fig. 3: A punctum adherens (green) fixing an astrocyte process (pale blue) to a mushroom-shaped dendritic spine possessing a perforated synapse (red). The spine (A) and astrocyte (B) made semitransparent to enable the punctum to be visible.

Extremely elaborated net-like vesicle-free adhesion junctions associated with synapses are formed between dendrites of thalamocortical projection neurons and giant axon terminals in synaptic glomerules of thalamic nuclei (Fig. 4).

Fig. 4: Reconstruction of extensively elaborated net-like vesicle-free adhesion junctions (yellow) associated with synaptic active zones (red) between a dendrite of thalamocortical relay neuron and a lemniscal giant axon terminal in thalamic ventrobasal nucleus of rat.

References:

Colman DR (1997) Minireview and hypothesis. Neurites, synapses, and cadherins reconciled. Molecular and Cellular Neuroscience 10:1-6.

Fannon AM, Colman DR (1996) A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron 17:423-434.

Lieberman AR, Spacek J (1997) Filamentous contacts: the ultrastructure and three-dimensional organization of specialized non-synaptic interneuronal appositions in thalamic relay nuclei. Cell Tiss. Res. 288:43-57.

Martin KC, Kandel ER (1996) Cell adhesion molecules, CREB, and the formation of new synaptic connections. Neuron 17:597-570.

Spacek J (1985b) Relationships between synaptic junctions, puncta adhaerentia and the spine apparatus at neocortical axo-spinous synapses. Anat. Embryol. 173:129-135.

Spacek J, Harris KM (1997) Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J.Neurosci. 17:190-203.

Spacek J, Harris KM (1998) Three-dimensional organization of cell adhesion junctions at synapses and dendritic spines in area CA1 of the rat hippocampus. J.Comp.Neurol. 393:58-68.

Uchida N, Honjo Y, Johnson KR, Wheelock MJ,Takeichi M (1996) The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J.Cell Biol. 135:767-779.

Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neuroscience 19(16):6897-6906.

Last Updated: 12/6/99