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Here, we develop a strategy combining compartment-specific crosslinking immunoprecipitation (CLIP) and translating ribosome affinity purification (TRAP) in conditionally tagged mice to precisely define the ribosome-bound dendritic transcriptome of CA1 pyramidal neurons. We identify CA1 dendritic transcripts with differentially localized mRNA isoforms generated by alternative polyadenylation and alternative splicing, including many that have altered protein-coding capacity. Among dendritic mRNAs, FMRP targets were found to be overrepresented. Cell-type-specific FMRP-CLIP and TRAP in microdissected CA1 neuropil revealed 383 dendritic FMRP targets and suggests that FMRP differentially regulates functionally distinct modules in CA1 dendrites and cell bodies. FMRP regulates ~15\u201320% of mRNAs encoding synaptic functions and 10% of chromatin modulators, in the dendrite and cell body, respectively. In the absence of FMRP, dendritic FMRP targets had increased ribosome association, consistent with a function for FMRP in synaptic translational repression. Conversely, downregulation of FMRP targets involved in chromatin regulation in cell bodies suggests a role for FMRP in stabilizing mRNAs containing stalled ribosomes in this compartment. Together, the data support a model in which FMRP regulates the translation and expression of synaptic and nuclear proteins within different compartments of a single neuronal cell type.<\/jats:p>","DOI":"10.7554\/elife.71892","type":"journal-article","created":{"date-parts":[[2021,12,23]],"date-time":"2021-12-23T10:06:05Z","timestamp":1640253965000},"update-policy":"https:\/\/doi.org\/10.7554\/elife.71892","source":"Crossref","is-referenced-by-count":65,"title":["FMRP regulates mRNAs encoding distinct functions in the cell body and dendrites of CA1 pyramidal neurons"],"prefix":"10.7554","volume":"10","author":[{"given":"Caryn R","family":"Hale","sequence":"first","affiliation":[{"name":"Laboratory of Molecular Neuro-Oncology, Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4195-6327","authenticated-orcid":true,"given":"Kirsty","family":"Sawicka","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Neuro-Oncology, Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kevin","family":"Mora","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Neuro-Oncology, Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John J","family":"Fak","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Neuro-Oncology, Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin Joo","family":"Kang","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Neuro-Oncology, Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paula","family":"Cutrim","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Neuro-Oncology, Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katarzyna","family":"Cialowicz","sequence":"additional","affiliation":[{"name":"Bio-Imaging Resource Center, The Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas S","family":"Carroll","sequence":"additional","affiliation":[{"name":"Bioinformatics Resource Center, The Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5134-8088","authenticated-orcid":true,"given":"Robert B","family":"Darnell","sequence":"additional","affiliation":[{"name":"Laboratory of Molecular Neuro-Oncology, Rockefeller University","place":["New York, United States"]},{"name":"Howard Hughes Medical Institute, Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4374","published-online":{"date-parts":[[2021,12,23]]},"reference":[{"key":"bib1","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms5510","article-title":"Functionally diverse dendritic mRNAs rapidly associate with ribosomes following a novel experience","volume":"5","author":"Ainsley","year":"2014","journal-title":"Nature Communications"},{"key":"bib2","doi-asserted-by":"publisher","first-page":"2008","DOI":"10.1101\/gr.133744.111","article-title":"Detecting differential usage of exons from RNA-seq data","volume":"22","author":"Anders","year":"2012","journal-title":"Genome Research"},{"key":"bib3","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1016\/j.tcb.2009.06.001","article-title":"To localize or not to localize: mRNA fate is in 3\u2019UTR ends","volume":"19","author":"Andreassi","year":"2009","journal-title":"Trends in Cell Biology"},{"key":"bib4","doi-asserted-by":"publisher","first-page":"1668","DOI":"10.1002\/ajmg.a.36902","article-title":"CNKSR2 deletions: a novel cause of X-linked intellectual disability and seizures","volume":"167","author":"Aypar","year":"2015","journal-title":"American Journal of Medical Genetics. 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