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The Journal of Neuroscience, October 7, 2009, 29(40):12449-12466; doi:10.1523/JNEUROSCI.1381-09.2009

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Cellular/Molecular
Rapid Assembly of Functional Presynaptic Boutons Triggered by Adhesive Contacts

Anna Lisa Lucido,^1,4 Fernando Suarez Sanchez,^2,4 Peter Thostrup,^2,4 Adam V. Kwiatkowski,⁵ Sergio Leal-Ortiz,⁶ Gopakumar Gopalakrishnan,^1,3,4 Dalinda Liazoghli,^1,4 Wiam Belkaid,^1,4 R. Bruce Lennox,^3,4 Peter Grutter,^2,4 Craig C. Garner,⁶ and David R. Colman^1,4

¹Montreal Neurological Institute and Hospital, McGill University, Montreal, Quebec H3A 2B4, Canada, ²Department of Physics, McGill University, Montreal, Quebec H3A 2T8, Canada, ³Department of Chemistry, McGill University, Montreal, Quebec H3A 2K6, Canada ⁴Program in NeuroEngineering, McGill University, Montreal, Quebec H3A 2B4, Canada, ⁵Department of Biological Sciences, Stanford University, Palo Alto, California 94305, and ⁶Department of Psychiatry and Behavioral Science, Nancy Pritzker Laboratory, Stanford University, Palo Alto, California 94304

Correspondence should be addressed to Dr. David R. Colman, Montreal Neurological Institute, McGill University, 3801 University Street, Room 636, Montreal, QC H3A 2B4, Canada. Email: david.colman{at}mcgill.ca

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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Received March 19, 2009; revised July 24, 2009; accepted Aug. 4, 2009.

Correspondence should be addressed to Dr. David R. Colman, Montreal Neurological Institute, McGill University, 3801 University Street, Room 636, Montreal, QC H3A 2B4, Canada. Email: david.colman{at}mcgill.ca

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