Species-dependent posttranscriptional regulation of NOS1 by FMRP in the developing cerebral cortex
Open accessAbstract
Fragile X syndrome (FXS), the leading monogenic cause of intellectual disability and autism, results from loss of function of the RNA-binding protein FMRP. Here, we show that FMRP regulates translation of neuronal nitric oxide synthase 1 (NOS1) in the developing human neocortex. Whereas NOS1 mRNA is widely expressed, NOS1 protein is transiently coexpressed with FMRP during early synaptogenesis in layer- and region-specific pyramidal neurons. These include midfetal layer 5 subcortically projecting neurons arranged into alternating columns in the prospective Broca's area and orofacial motor cortex. Human NOS1 translation is activated by FMRP via interactions with coding region binding motifs absent from mouse Nos1 mRNA, which is expressed in mouse pyramidal neurons, but not efficiently translated. Correspondingly, neocortical NOS1 protein levels are severely reduced in developing human FXS cases, but not FMRP-deficient mice. Thus, alterations in FMRP posttranscriptional regulation of NOS1 in developing neocortical circuits may contribute to cognitive dysfunction in FXS.
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FMRP is not only involved in translational repression, it is also a translational enhancer.
“Indeed, FMRP is not only involved in translational repression, it is also a translational enhancer (Bechara et al., 2009; Gross et al., 2011; Kwan et al., 2012; Tabet et al., 2016)”
From New insights into the regulatory function of CYFIP1 in the context of WAVE- and FMRP-containing complexes (2017) · cites this paper as Kwan et al., 2012
The earliest synapses within the cortical plate are observed around 18 postconceptional weeks, terminating on prospective layer 5 projection neurons.
“The earliest synapses within the CP are observed around 18 pcw, terminating on prospective layer 5 projection (pyramidal) neurons (Kwan et al., 2012).”
From The Cellular and Molecular Landscapes of the Developing Human Central Nervous System (2016) · cites this paper as Kwan et al., 2012
Studies of postmortem brains of individuals with autism spectrum disorder or fragile X syndrome have revealed distinct spatio-temporal patterns of transcriptional and post-transcriptional dysregulation.
“Recent studies of the developing postmortem human brains of individuals affected with autism spectrum disorder or fragile X syndrome have revealed distinct spatio-temporal patterns of transcriptional and post-transcriptional dysregulation (Kwan et al., 2012; Voineagu et al., 2011).”
From The Cellular and Molecular Landscapes of the Developing Human Central Nervous System (2016) · cites this paper as Kwan et al., 2012
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Kraushar, M. L., Thompson, K., Wijeratne, H. R. S., Viljetic, B., Sakers, K., Marson, J. W., Kontoyiannis, D. L., Buyske, S., Hart, R. P., & Rasin, M.-R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1408305111 · Cited by 98 · see citing works
Revisiting enigmatic cortical calretinin-expressing interneurons
Cauli, B., Zhou, X., Tricoire, L., Toussay, X., & Staiger, J. F. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00052 · Cited by 86 · see citing works
Abekhoukh, S., Sahin, H. B., Grossi, M., Zongaro, S., Maurin, T., Madrigal, I., Kazue-Sugioka, D., Raas-Rothschild, A., Doulazmi, M., Carrera, P., et al. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.025809 · Cited by 59 · see citing works
“Indeed, FMRP is not only involved in translational repression, it is also a translational enhancer (Bechara et al., 2009; Gross et al., 2011; Kwan et al., 2012; Tabet et al., 2016) and a translation-independent function was also described for FMRP (Myrick et al., 2015).”
Micali, N., Kim, S.-K., Diaz-Bustamante, M., Stein-O’Brien, G., Seo, S., Shin, J.-H., Rash, B. G., Ma, S., Wang, Y., Olivares, N. A., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107599 · Cited by 31 · see citing works
Self-citationConsequences of trisomy 21 for brain development in Down syndrome
Russo, M. L., Sousa, A. M. M., & Bhattacharyya, A. (2024) · Nature Reviews Neuroscience · doi:10.1038/s41583-024-00866-2 · Cited by 28 · see citing works
Self-citation
- Authors
- Kwan, K. Y., Lam, M. M. S., Johnson, M. B., Dube, U., Shim, S., Rašin, M.-R., Sousa, A. M. M., Fertuzinhos, S., Chen, J.-G., Arellano, J. I., Chan, D. W., Pletikos, M., Vasung, L., Rowitch, D. H., Huang, E. J., Schwartz, M. L., Willemsen, R., Oostra, B. A., Rakic, P., Heffer, M., Kostović, I., Judaš, M., & Šestan, N.
- Affiliations
- Yale University (US)
- Universidade do Porto (PT)
- Wenzhou Medical University (CN)
- University of Zagreb (HR)
- Howard Hughes Medical Institute (US)
- University of California, San Francisco (US)
- Erasmus MC (NL)
- University of Osijek (HR)
- Corresponding author
- Šestan, Nenad
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2012-05
- Volume
- 149
- Issue
- 4
- Pages
- 899-911
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3351852
- OpenAlex
- W2022976940
- Cited by
- 137
- References
- 79
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 3 · 2023: 10 · 2022: 6 · 2021: 9 · 2020: 11 · 2019: 7 · 2018: 11 · 2017: 12 · 2016: 10 · 2015: 16 · 2014: 17 · 2013: 12 · 2012: 6
- FWCI
- 9.80
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- ZonMw
- National Institutes of Health (DA023999)
- University of California, San Francisco
- Office of the President, University of California (142675)
- National Institute of Mental Health (RC2MH089929, MH081896, MH089929, U01MH081896)
- National Institute on Drug Abuse (DA023999, R37DA023999)
- National Institute of Neurological Disorders and Stroke (R01NS054273, U24NS051869, NS 054273, R01NS014841, K99NS064303)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Keywords
- FMRP, NOS1, fragile X syndrome, post-transcriptional regulation, translational regulation, human neocortex development, pyramidal neurons, synaptogenesis, Broca's area, species differences, autism spectrum disorder, intellectual disability
- MeSH terms
- Animals, Cerebral Cortex, Fragile X Syndrome, Gene Expression Regulation, Humans, RNA Processing, Post-Transcriptional, Species Specificity, Pyramidal Cells, Mice, Knockout, Mice, Fragile X Messenger Ribonucleoprotein 1, Nitric Oxide Synthase Type I, Neurogenesis
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