Developmental Changes in Peripherin-eGFP Expression in Spiral Ganglion Neurons

. 2021 ; 15 () : 678113. [epub] 20210615

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34211371

The two types of spiral ganglion neurons (SGNs), types I and II, innervate inner hair cells and outer hair cells, respectively, within the mammalian cochlea and send another process back to cochlear nuclei in the hindbrain. Studying these two neuronal types has been made easier with the identification of unique molecular markers. One of these markers, peripherin, was shown using antibodies to be present in all SGNs initially but becomes specific to type II SGNs during maturation. We used mice with fluorescently labeled peripherin (Prph-eGFP) to examine peripherin expression in SGNs during development and in aged mice. Using these mice, we confirm the initial expression of Prph-eGFP in both types I and II neurons and eventual restriction to only type II perikarya shortly after birth. However, while Prph-eGFP is uniquely expressed within type II cell bodies by P8, both types I and II peripheral and central processes continue to express Prph-eGFP for some time before becoming downregulated. Only at P30 was there selective type II Prph-eGFP expression in central but not peripheral processes. By 9 months, only the type II cell bodies and more distal central processes retain Prph-eGFP expression. Our results show that Prph-eGFP is a reliable marker for type II SGN cell bodies beyond P8; however, it is not generally a suitable marker for type II processes, except for central processes beyond P30. How the changes in Prph-eGFP expression relate to subsequent protein expression remains to be explored.

Zobrazit více v PubMed

Berglund A. M., Ryugo D. K. (1987). Hair cell innervation by spiral ganglion neurons in the mouse. J. Comp. Neurol. 255 560–570. 10.1002/cne.902550408 PubMed DOI

Brown M., Berglund A., Kiang N., Ryugo D. K. (1988). Central trajectories of type II spiral ganglion neurons. J. Comparat. Neurol. 278 581–590. 10.1002/cne.902780409 PubMed DOI

Coate T. M., Kelley M. W. (2013). Making connections in the inner ear: recent insights into the development of spiral ganglion neurons and their connectivity with sensory hair cells. Semin. Cell Dev. Biol. 24 460–469. 10.1016/j.semcdb.2013.04.003 PubMed DOI PMC

Cragg B. (1980). Preservation of extracellular space during fixation of the brain for electron microscopy. Tissue Cell 12 63–72. 10.1016/0040-8166(80)90052-x PubMed DOI

Defourny J., Poirrier A. L., Lallemend F., Sánchez S. M., Neef J., Vanderhaeghen P., et al. (2013). Ephrin-A5/EphA4 signalling controls specific afferent targeting to cochlear hair cells. Nat. Commun. 4:1438. 10.1038/ncomms2445 PubMed DOI

De No R. L. (1981). The Primary Acoustic Nuclei. Philadelphia: Raven Press.

Erway L. C., Shiau Y.-W., Davis R. R., Krieg E. F. (1996). Genetics of age-related hearing loss in mice. III. Susceptibility of inbred and F1 hybrid strains to noise-induced hearing loss. Hear. Res. 93 181–187. 10.1016/0378-5955(95)00226-x PubMed DOI

Escurat M., Djabali K., Gumpel M., Gros F., Portier M. J. (1990). Differential expression of two neuronal intermediate-filament proteins, peripherin and the low-molecular-mass neurofilament protein (NF-L), during the development of the rat. J. Neurosci. 10 764–784. 10.1523/jneurosci.10-03-00764.1990 PubMed DOI PMC

Filova I., Dvorakova M., Bohuslavova R., Pavlinek A., Elliott K. L., Vochyanova S., et al. (2020). Combined atoh1 and neurod1 deletion reveals autonomous growth of auditory nerve fibers. Mol. Neurobiol. 57 5307–5323. 10.1007/s12035-020-02092-0 PubMed DOI PMC

Fritzsch B. (1979). Observations on degenerative changes of Purkinje cells during early development in mice and in normal and otocyst-deprived chickens. Anat. Embryol. 158 95–102. 10.1007/bf00315954 PubMed DOI

Fritzsch B., Elliott K. L., Pavlinkova G. (2019). Primary sensory map formations reflect unique needs and molecular cues specific to each sensory system. F1000Research 8:F1000FacultyRev-1345. PubMed PMC

Fritzsch B., Fariñas I., Reichardt L. F. (1997). Lack of neurotrophin 3 causes losses of both classes of spiral ganglion neurons in the cochlea in a region-specific fashion. J. Neurosci. 17 6213–6225. 10.1523/jneurosci.17-16-06213.1997 PubMed DOI PMC

Froud K. E., Wong A. C., Cederholm J. M., Klugmann M., Sandow S. L., Julien J. P., et al. (2015). Type II spiral ganglion afferent neurons drive medial olivocochlear reflex suppression of the cochlear amplifier. Nat. Commun. 6:7115. PubMed PMC

Grandi F. C., De Tomasi L., Mustapha M. (2020). Single-Cell RNA analysis of Type I spiral ganglion neurons reveals a Lmx1a population in the cochlea. Front. Mol. Neurosci. 13:83. 10.3389/fnmol.2020.00083 PubMed DOI PMC

Guinan J. J., Jr., Gifford M. L. (1988). Effects of electrical stimulation of efferent olivocochlear neurons on cat auditory-nerve fibers. I. Rate-level functions. Hear. Res. 33 97–113. 10.1016/0378-5955(88)90023-8 PubMed DOI

Hafidi A. (1998). Peripherin-like immunoreactivity in type II spiral ganglion cell body and projections. Brain Res. 805 181–190. 10.1016/s0006-8993(98)00448-x PubMed DOI

Hafidi A., Despres G., Romand R. (1993). Ontogenesis of type II spiral ganglion neurons during development: peripherin immunohistochemistry. Int. J. Dev. Neurosci. 11 507–512. 10.1016/0736-5748(93)90024-8 PubMed DOI

Johnson K. R., Zheng Q. Y., Erway L. C. (2000). A major gene affecting age-related hearing loss is common to at least ten inbred strains of mice. Genomics 70 171–180. 10.1006/geno.2000.6377 PubMed DOI

Kopecky B., Santi P., Johnson S., Schmitz H., Fritzsch B. (2011). Conditional deletion of N-Myc distrupts neurosensory and non-sensory development of the ear. Dev. Dynam. 240 1373–1390. 10.1002/dvdy.22620 PubMed DOI PMC

Lariviere R. C., Julien J. P. (2004). Functions of intermediate filaments in neuronal development and disease. J. Neurobiol. 58 131–148. 10.1002/neu.10270 PubMed DOI

Leonard R. B., Kevetter G. A. (2002). Molecular probes of the vestibular nerve: I. Peripheral termination patterns of calretinin, calbindin and peripherin containing fibers. Brain Res. 928 8–17. 10.1016/s0006-8993(01)03268-1 PubMed DOI

Maison S., Liberman L. D., Liberman M. C. (2016). Type II cochlear ganglion neurons do not drive the olivocochlear reflex: Re-examination of the cochlear phenotype in peripherin knock-out mice. eNeuro 3. 10.1523/ENEURO.0207-16.2016 PubMed DOI PMC

McLenachan S., Goldshmit Y., Fowler K. J., Voullaire L., Holloway T. P., Turnley A. M., et al. (2008). Transgenic mice expressing the Peripherin-EGFP genomic reporter display intrinsic peripheral nervous system fluorescence. Transgenic Res. 17 1103–1116. 10.1007/s11248-008-9210-7 PubMed DOI

Nayagam B. A., Muniak M. A., Ryugo D. K. (2011). The spiral ganglion: connecting the peripheral and central auditory systems. Hear. Res. 278 2–20. 10.1016/j.heares.2011.04.003 PubMed DOI PMC

Petitpre C., Wu H., Sharma A., Tokarska A., Fontanet P., Wang Y., et al. (2018). Neuronal heterogeneity and stereotyped connectivity in the auditory afferent system. Nat. Commun. 9:3691. PubMed PMC

Rubel E. W., Fritzsch B. (2002). Auditory system development: primary auditory neurons and their targets. Annu. Rev. Neurosci. 25 51–101. 10.1146/annurev.neuro.25.112701.142849 PubMed DOI

Schmidt H., Fritzsch B. (2019). Npr2 null mutants show initial overshooting followed by reduction of spiral ganglion axon projections combined with near-normal cochleotopic projection. Cell Tissue Res. 378 15–32. 10.1007/s00441-019-03050-6 PubMed DOI PMC

Shrestha B. R., Chia C., Wu L., Kujawa S. G., Liberman M. C., Goodrich L. V. (2018). Sensory neuron diversity in the inner ear is shaped by activity. Cell 174 1229–1246.e1217. PubMed PMC

Simmons D. D., Liberman M. C. (1988). Afferent innervation of outer hair cells in adult cats: I. Light microscopic analysis of fibers labeled with horseradish peroxidase. J. Comp. Neurol. 270 132–144. 10.1002/cne.902700111 PubMed DOI

Spoendlin H. (1971). Degeneration behaviour of the cochlear nerve. Archiv. Klinische Exper. Ohren Nasen Kehlkopfheilkunde 200 275–291. 10.1007/bf00373310 PubMed DOI

Sun S., Babola T., Pregernig G., So K. S., Nguyen M., Su S. M., et al. (2018). Hair cell mechanotransduction regulates spontaneous activity and spiral ganglion subtype specification in the auditory system. Cell 174 1247–1263.e1215. PubMed PMC

Vyas P., Wu J. S., Jimenez A., Glowatzki E., Fuchs P. A. (2019). Characterization of transgenic mouse lines for labeling type I and type II afferent neurons in the cochlea. Sci. Rep. 9:5549. PubMed PMC

Vyas P., Wu J. S., Zimmerman A., Fuchs P., Glowatzki E. (2017). Tyrosine Hydroxylase expression in Type II cochlear afferents in mice. J. Assoc. Res. Otolaryngol. 18 139–151. 10.1007/s10162-016-0591-7 PubMed DOI PMC

Weisz C., Glowatzki E., Fuchs P. (2009). The postsynaptic function of type II cochlear afferents. Nature 461 1126–1129. 10.1038/nature08487 PubMed DOI PMC

Wu J. S., Vyas P., Glowatzki E., Fuchs P. A. (2018). Opposing expression gradients of calcitonin-related polypeptide alpha (Calca/Cgrpalpha) and tyrosine hydroxylase (Th) in type II afferent neurons of the mouse cochlea. J. Comp. Neurol. 526:1073. 10.1002/cne.24380 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...