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Although numerous signals are known to regulate synapses, it remains unclear which signaling mechanisms organize initial synapse assembly. Here, we describe new tools, referred to as \u201cSynTAMs\u201d for synaptic targeting molecules, that enable localized perturbations of cAMP signaling in developing postsynaptic specializations. We show that locally restricted suppression of postsynaptic cAMP levels or of cAMP-dependent protein-kinase activity severely impairs excitatory synapse formation without affecting neuronal maturation, dendritic arborization, or inhibitory synapse formation. In vivo, suppression of postsynaptic cAMP signaling in CA1 neurons prevented formation of both Schaffer-collateral and entorhinal-CA1\/temporoammonic-path synapses, suggesting a general principle. Retrograde trans-synaptic rabies virus tracing revealed that postsynaptic cAMP signaling is required for continuous replacement of synapses throughout life. Given that postsynaptic latrophilin adhesion-GPCRs drive synapse formation and produce cAMP, we suggest that spatially restricted postsynaptic cAMP signals organize assembly of postsynaptic specializations during synapse formation.<\/jats:p>","DOI":"10.1083\/jcb.202109111","type":"journal-article","created":{"date-parts":[[2021,12,16]],"date-time":"2021-12-16T13:40:27Z","timestamp":1639662027000},"update-policy":"https:\/\/doi.org\/10.1083\/jcb.crossmarkpolicy","source":"Crossref","is-referenced-by-count":23,"title":["Engineered synaptic tools reveal localized cAMP signaling in synapse assembly"],"prefix":"10.1083","volume":"221","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1797-2346","authenticated-orcid":true,"given":"Richard","family":"Sando","sequence":"first","affiliation":[{"name":"Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA 1"},{"name":"Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA 2"},{"name":"Department of Pharmacology, Vanderbilt University, Nashville, TN 3"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Milan Lyndie","family":"Ho","sequence":"additional","affiliation":[{"name":"Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA 1"},{"name":"Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA 2"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1586-2151","authenticated-orcid":true,"given":"Xinran","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Yale University School of Medicine, New Haven, CT 4"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3361-9275","authenticated-orcid":true,"given":"Thomas C.","family":"S\u00fcdhof","sequence":"additional","affiliation":[{"name":"Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA 1"},{"name":"Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA 2"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"291","published-online":{"date-parts":[[2021,12,16]]},"reference":[{"key":"2023072418591041600_bib1","doi-asserted-by":"publisher","first-page":"3831","DOI":"10.1083\/jcb.201703042","article-title":"Postsynaptic adhesion GPCR latrophilin-2 mediates target recognition in entorhinal-hippocampal synapse assembly","volume":"216","author":"Anderson","year":"2017","journal-title":"J. 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