Rapid assembly of functional presynaptic boutons triggered by adhesive contacts.
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.
Lucido
Anna Lisa
AL
Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec H3A 2B4, Canada.
Suarez Sanchez
Fernando
F
Thostrup
Peter
P
Kwiatkowski
Adam V
AV
Leal-Ortiz
Sergio
S
Gopalakrishnan
Gopakumar
G
Liazoghli
Dalinda
D
Belkaid
Wiam
W
Lennox
R Bruce
RB
Grutter
Peter
P
Garner
Craig C
CC
Colman
David R
DR
D000818:Animals; D001369:Axons; D002448:Cell Adhesion; D002478:Cells, Cultured; D006624:Hippocampus / Q000166:cytology* / Q000196:embryology / Q000378:metabolism*; D008565:Membrane Proteins / Q000378:metabolism; D018625:Microscopy, Atomic Force; D018613:Microscopy, Confocal; D017729:Presynaptic Terminals / Q000378:metabolism* / Q000648:ultrastructure*; D051381:Rats; D017207:Rats, Sprague-Dawley; D013572:Synaptic Vesicles / Q000378:metabolism / Q000648:ultrastructure
D008565:Membrane Proteins