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The Journal of Neuroscience, August 17, 2005, 25(33):7517-7528; doi:10.1523/JNEUROSCI.2010-05.2005

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Cellular/Molecular
The Two Isoforms of the Caenorhabditis elegans Leukocyte-Common Antigen Related Receptor Tyrosine Phosphatase PTP-3 Function Independently in Axon Guidance and Synapse Formation

Brian D. Ackley,^1,2 Robert J. Harrington,¹ Martin L. Hudson,¹ Lisa Williams,³ Cynthia J. Kenyon,³ Andrew D. Chisholm,¹ and Yishi Jin^1,2

¹Sinsheimer Laboratories, Department of Molecular, Cellular, and Developmental Biology, University of California-Santa Cruz, Santa Cruz, California 95064, ²Howard Hughes Medical Institute, Santa Cruz, California 95064, and ³Department of Biophysics and Biochemistry, University of California-San Francisco, San Francisco, California 94143

Leukocyte-common antigen related (LAR)-like phosphatase receptors are conserved cell adhesion molecules that function in multiple developmental processes. The Caenorhabditis elegans ptp-3 gene encodes two LAR family isoforms that differ in the extracellular domain. We show here that the long isoform, PTP-3A, localizes specifically at synapses and that the short isoform, PTP-3B, is extrasynaptic. Mutations in ptp-3 cause defects in axon guidance that can be rescued by PTP-3B but not by PTP-3A. Mutations that specifically affect ptp-3A do not affect axon guidance but instead cause alterations in synapse morphology. Genetic double-mutant analysis is consistent with ptp-3A acting with the extracellular matrix component nidogen, nid-1, and the intracellular adaptor -liprin, syd-2. nid-1 and syd-2 are required for the recruitment and stability of PTP-3A at synapses, and mutations in ptp-3 or nid-1 result in aberrant localization of SYD-2. Overexpression of PTP-3A is able to bypass the requirement for nid-1 for the localization of SYD-2 and RIM. We propose that PTP-3A acts as a molecular link between the extracellular matrix and -liprin during synaptogenesis.

Key words: synaptogenesis; axon guidance; cell adhesion; -liprin; syd-2; LAR receptor tyrosine phosphatase; nidogen

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Received May 18, 2005; revised June 24, 2005; accepted June 28, 2005.

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