Development of presynaptic specializations induced by basic polypeptide‐coated latex beads in spinal cord cultures

Peng, H. Benjamin; Markey, Donald R.; Muhlach, William L.; Pollack, Emanuel D.

doi:10.1002/syn.890010104

Cited by 26 publications

(20 citation statements)

References 39 publications

(39 reference statements)

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“…PDL-coated beads induce membrane adhesion followed by the subplasmalemmal clustering of synaptic vesicle complexes under the adhesion site within axons Previous studies (Burry, 1980(Burry, , 1982Peng et al, 1987) revealed that cultures of cerebellar granule cells were capable of forming contact-induced clusters of vesicles within 24 h on PLL-coated beads. To further investigate this phenomenon, low-density hippocampal cultures were grown (to DIV7, DIV15, or DIV21) and thereafter incubated with 7 m polystyrene beads coated with PDL (50 g/ml) (supplemental Fig.…”

Section: Resultsmentioning

confidence: 99%

“…The pooled fluorescence ratios are also shown for each category. 1982, 1983, 1985Peng et al, 1987). Because substrates were necessarily polybasic for the clustering effect to occur, it was concluded that electrostatic-based adhesion between an axon and its target represents the first step that triggers synapse assembly (Burry, 1980).…”

Section: Discussionmentioning

confidence: 99%

“…Although the SV clustering phenomenon had been described previously (Burry, 1980(Burry, , 1982Peng et al, 1987), it was unclear whether or not these bouton-like structures contained active zones indicative of functional bona fide presynaptic endings. This was first explored by immunostaining cultures of hippocampal neurons, grown for 15 DIV, and incubated with beads for 24 h, with antibodies against a variety of SV and active zone markers ( Fig.…”

Section: Pdl-coated Beads Induce the Formation Of Functional Presynapmentioning

confidence: 95%

“…The ensuing presynaptic specializations formed between neuronal processes and PDL-coated beads are more than simple SVfilled varicosities (Burry, 1980(Burry, , 1982Peng et al, 1987), but functional excitatory or inhibitory presynapses. These bead-presynaptic complexes are highly stable, unlike the mobile presynaptic-like clusters observed along isolated axons (Krueger et al, 2003).…”

Section: Presynaptic Complexes Are True Boutons Not Mere Synaptic Vementioning

confidence: 99%

“…The paradigm is based on earlier observations showing that cultured cerebellar neurons form presynaptic-like specializations when placed in contact with beads coated with positively charged proteins including poly-L-lysine (PLL) and argininerich histones, but not with beads coated with negative or neutral charge (Burry, 1980(Burry, , 1982Peng et al, 1987). These studies imply that target adhesion alone can trigger presynaptic endings to form in the absence of any specialized cues.…”

Section: Introductionmentioning

confidence: 99%

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Rapid Assembly of Functional Presynaptic Boutons Triggered by Adhesive Contacts

Lucido¹,

Sanchez²,

Thostrup³

et al. 2009

J. Neurosci.

127

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CNS synapse assembly typically follows after stable contacts between "appropriate" axonal and dendritic membranes are made. We show that presynaptic boutons selectively form de novo following neuronal fiber adhesion to beads coated with poly-D-lysine (PDL), an artificial cationic polypeptide. As demonstrated by atomic force and live confocal microscopy, functional presynaptic boutons self-assemble as rapidly as 1 h after bead contact, and are found to contain a variety of proteins characteristic of presynaptic endings. Interestingly, presynaptic compartment assembly does not depend on the presence of a biological postsynaptic membrane surface. Rather, heparan sulfate proteoglycans, including syndecan-2, as well as others possibly adsorbed onto the bead matrix or expressed on the axon surface, are required for assembly to proceed by a mechanism dependent on the dynamic reorganization of F-actin. Our results indicate that certain (but not all) nonspecific cationic molecules like PDL, with presumably electrostatically mediated adhesive properties, can effectively bypass cognate and natural postsynaptic ligands to trigger presynaptic assembly in the absence of specific target recognition. In contrast, we find that postsynaptic compartment assembly depends on the prior presence of a mature presynaptic ending.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Pdl-coated Beads Induce the Formation Of Functional Presynapmentioning

confidence: 95%

Section: Presynaptic Complexes Are True Boutons Not Mere Synaptic Vementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Rapid Assembly of Functional Presynaptic Boutons Triggered by Adhesive Contacts

Lucido¹,

Sanchez²,

Thostrup³

et al. 2009

J. Neurosci.

127

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Laminins and human disease

McGowan

Marinkovich

2000

Microsc. Res. Tech.

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The laminin protein family has diverse tissue expression patterns and is involved in the pathology of a number of organs, including skin, muscle, and nerve. In the skin, laminins 5 and 6 contribute to dermal‐epidermal cohesion, and mutations in the constituent chains result in the blistering phenotype observed in patients with junctional epidermolysis bullosa (JEB). Allelic heterogeneity is observed in patients with JEB: mutations that results in premature stop codons produce a more severe phenotype than do missense mutations. Gene therapy approaches are currently being studied in the treatment of this disease. A blistering phenotype is also observed in patients with acquired cicatricial pemphigoid (CP). Autoantibodies targeted against laminins 5 and 6 destabilize epithelial adhesion and are pathogenic. In muscle cells, laminin α2 is a component of the bridge that links the actin cytoskeleton to the extracellular matrix. In patients with laminin α2 mutations, the bridge is disrupted and mature muscle cells apoptose. Congenital muscular dystrophy (CMD) results. The role of laminin in diseases of the nervous system is less well defined, but the extracellular protein has been shown to serve an important role in peripheral nerve regeneration. The adhesive molecule influences neurite outgrowth, neural differentiation, and synapse formation. The broad spatial distribution of laminin gene products suggests that laminin may be involved in a number of diseases for which pathogenic mechanisms are still being unraveled. Microsc. Res. Tech. 51:262–279, 2000. © 2000 Wiley‐Liss, Inc.

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Development of calcitonin gene‐related peptide (CGRP) immunoreactivity in relationship to the formation of neuromuscular junctions in Xenopus myotomal muscle

Peng

Chen

Biasi

et al. 1989

J of Comparative Neurology

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Immunoreactivity (IR) to calcitonin gene-related peptide (CGRP) has recently been found in chick motoneurons. Bath application of this peptide causes an increase in surface acetylcholine receptor (AChR) density and cAMP level in cultured chick muscle cells. These results suggest a role for this peptide in the formation of synaptic specializations. In this study, we examined the development of CGRP IR in larval Xenopus myotomal muscle in relation to synaptogenesis. Using an antiserum against CGRP, a monoclonal antibody against the p65 synaptic vesicle antigen and a fluorescence conjugate of alpha-bungarotoxin, we followed the development of synaptic specializations with fluorescence microscopy in whole-mount specimens. We found that the postsynaptic specialization in the form of AChR clusters was first detected in stage 22 (24 hour) embryos. The presynaptic specializations, including the synaptic vesicle clusters as evidenced by p65 antibody staining and CGRP IR, were first detected at stage 32 (40 hours). The appearance of these two presynaptic specializations followed the same time course. Subsequently, all three structures, the AChR clusters, CGRP IR, and synaptic vesicle clusters, were colocalized at the neuromuscular junction (NMJ). This shows that CGRP is unlikely to be involved in signaling the development of the postsynaptic apparatus. This premise is further examined in cultures of Xenopus myotomal muscle cells. CGRP at concentrations up to 1 microM did not affect the number of AChR clusters, nor did it interfere with the formation of clusters induced by polycation-coated beads. In contrast, an extract from the basement membrane of Torpedo electric organ promoted the formation of AChR clusters and interfered with the clustering activity of the beads. These results suggest that CGRP, an integral component of the presynaptic specialization, is not involved in signaling synaptogenesis at the NMJ.

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Development of presynaptic specializations induced by basic polypeptide‐coated latex beads in spinal cord cultures

Cited by 26 publications

References 39 publications

Rapid Assembly of Functional Presynaptic Boutons Triggered by Adhesive Contacts

Rapid Assembly of Functional Presynaptic Boutons Triggered by Adhesive Contacts

Laminins and human disease

Development of calcitonin gene‐related peptide (CGRP) immunoreactivity in relationship to the formation of neuromuscular junctions in Xenopus myotomal muscle

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