Intense and specialized dendritic localization of the fragile X mental retardation protein in binaural brainstem neurons: a comparative study in the alligator, chicken, gerbil, and human
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Neuronal dendrites are structurally and functionally dynamic in response to changes in afferent activity. The fragile X mental retardation protein (FMRP) is an mRNA binding protein that regulates activity‐dependent protein synthesis and morphological dynamics of dendrites. Loss and abnormal expression of FMRP occur in fragile X syndrome (FXS) and some forms of autism spectrum disorders. To provide further understanding of how FMRP signaling regulates dendritic dynamics, we examined dendritic expression and localization of FMRP in the reptilian and avian nucleus laminaris (NL) and its mammalian analogue, the medial superior olive (MSO), in rodents and humans. NL/MSO neurons are specialized for temporal processing of low‐frequency sounds for binaural hearing, which is impaired in FXS. Protein BLAST analyses first demonstrate that the FMRP amino acid sequences in the alligator and chicken are highly similar to human FMRP with identical mRNA‐binding and phosphorylation sites, suggesting that FMRP functions similarly across vertebrates. Immunocytochemistry further reveals that NL/MSO neurons have very high levels of dendritic FMRP in low‐frequency hearing vertebrates including alligator, chicken, gerbil, and human. Remarkably, dendritic FMRP in NL/MSO neurons often accumulates at branch points and enlarged distal tips, loci known to be critical for branch‐specific dendritic arbor dynamics. These observations support an important role for FMRP in regulating dendritic properties of binaural neurons that are essential for low‐frequency sound localization and auditory scene segregation, and support the relevance of studying this regulation in nonhuman vertebrates that use low frequencies in order to further understand human auditory processing disorders. J. Comp. Neurol. 522:2107–2128, 2014. © 2013 Wiley Periodicals, Inc.
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FMRP is expressed throughout the auditory system, and the cortical habituation deficits may have multiple origins (Strumbos et al., 2010; Wang et al., 2014; Rotschafer et al., 2015).
“However, FMRP is expressed across the auditory system and the observed cortical habituation deficits may have multiple origins (Strumbos et al., 2010; Wang et al., 2014; Rotschafer et al., 2015).”
From Matrix metalloproteinase-9 deletion rescues auditory evoked potential habituation deficit in a mouse model of Fragile X Syndrome (2016) · cites this paper as Wang et al., 2014
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Tobia, M. J., & Woodruff‐Pak, D. S. (2009) · Behavioral Neuroscience · doi:10.1037/a0015662 · Cited by 17 · see citing works
In VivoReversible Regulation of Dendritic Patterning by Afferent Input in Bipolar Auditory Neurons
Wang, Y., & Rubel, E. W. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1737-12.2012 · Cited by 17 · see citing works
Self-citationProbing Astrocyte Function in Fragile X Syndrome
Jacobs, S. A., Cheng, C., & Doering, L. C. (2011) · Results and problems in cell differentiation · doi:10.1007/978-3-642-21649-7_2 · Cited by 15 · see citing works
Wang, Y., Cunningham, D. E., Tempel, B. L., & Rubel, E. W. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22045 · Cited by 15 · see citing works
Self-citationOxidative stress reveals heterogeneity of FMRP granules in PC12 cell neurites
Dolzhanskaya, N., Merz, G., & Denman, R. B. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.026 · Cited by 14 · see citing works
Relative input strength rapidly regulates dendritic structure of chick auditory brainstem neurons
Sorensen, S. A., & Rubel, E. W. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22656 · Cited by 12 · see citing works
Self-citationMcBride, E. G., Rubel, E. W., & Wang, Y. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23227 · Cited by 11 · see citing works
Self-citationBrain-stem auditory evoked potentials in the fragile X syndrome.
Ferri, R. (1989) · PubMed · Cited by 10 · see citing works
Editorial: Pragmatics and statistics in psychiatric genetics
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Wang, Y., Sanchez, J. T., & Rubel, E. W. (2010) · Oxford University Press eBooks · doi:10.1093/med/9780195389883.003.0022 · Cited by 4 · see citing works
Self-citationIrwin (2001) · doi:10.1002/1096-8628(20010115)98:2
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Sinclair, D., Oranje, B., Razak, K. A., Siegel, S. J., & Schmid, S. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.029 · Cited by 198 · see citing works
“FMRP is expressed across multiple levels of the auditory neuraxis (Wang et al., 2014).”
Lovelace, J. W., Wen, T. H., Reinhard, S., Hsu, M. S., Sidhu, H., Ethell, I. M., Binder, D. K., & Razak, K. A. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.02.002 · Cited by 115 · see citing works
Deletion of Fmr1 alters function and synaptic inputs in the auditory brainstem
Rotschafer, S. E., Marshak, S., & Cramer, K. S. (2015) · PLOS ONE · doi:10.1371/journal.pone.0117266 · Cited by 72 · see citing works
Garcia-Pino, E., Gessele, N., & Koch, U. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2310-16.2017 · Cited by 58 · see citing works
- Authors
- Wang, Y., Sakano, H., Beebe, K., Brown, M. R., de Laat, R., Bothwell, M., Kulesza, R. J., & Rubel, E. W.
- Affiliations
- University of Washington (US)
- Lake Erie College of Osteopathic Medicine (US)
- Yale University (US)
- Institute for Stem Cell and Regenerative Medicine and Department of Physiology and Biophysics University of Washington Seattle WA 98109
- Corresponding author
- Rubel, Edwin W
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2014-04-19
- Volume
- 522
- Issue
- 9
- Pages
- 2107-2128
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- PMC
- PMC5564206
- OpenAlex
- W2103174972
- Cited by
- 40
- References
- 106
- Citations by year
- 2025: 2 · 2024: 1 · 2023: 4 · 2022: 4 · 2021: 3 · 2020: 5 · 2019: 3 · 2018: 3 · 2017: 5 · 2016: 5 · 2015: 3 · 2014: 2
- FWCI
- 2.21
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Deafness and Other Communication Disorders (DC-03829, DC-02739, DC04661, DC 00018, R01DC013074, R21DC011594, R01DC003829, R01DC002739, T32DC000018, DC-011594, P30DC004661)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
- Keywords
- FMRP, dendritic localization, nucleus laminaris, medial superior olive, binaural hearing, fragile X syndrome, autism spectrum disorder, comparative neurobiology, alligators, chickens, gerbils, human
- MeSH terms
- Aged, Aged, 80 and over, Alligators and Crocodiles, Animals, Brain Stem, Chickens, Dendrites, Female, Gerbillinae, Humans, Male, Middle Aged, Species Specificity, Rats, Sprague-Dawley, Sequence Homology, Amino Acid, Avian Proteins, Reptilian Proteins, Fragile X Messenger Ribonucleoprotein 1, Superior Olivary Complex
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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