Skip to main content
Log in

Neuronal expression of peripherin, a type III intermediate filament protein, in the mouse hindbrain

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

Peripherin is a 57 kDa Type III intermediate filament protein associated with neurite extension, neuropathies such as amyotrophic lateral sclerosis, and cranial nerve and dorsal root projections. However, knowledge of peripherin expression in the CNS is limited. We have used immunoperoxidase histochemistry to characterise peripherin expression in the mouse hindbrain, including the inferior colliculus, pons, medulla and cerebellum. Peripherin immunolabelling was observed in the nerve fibres and nuclei that are associated with all cranial nerves [(CN) V–XII] in the hindbrain. Peripherin expression was prominent in the cell bodies and axons of the mesenchephalic trigeminal nucleus and the pars compacta region of nucleus ambiguus, and in the fibres that comprise the solitary tract, the descending spinal trigeminal tract and the trigeminal and facial nerves. A small proportion of peripherin positive fibres in CN VIII likely arise from cochlear type II spiral ganglion neurons. Peripherin positive fibres were also observed in the inferior cerebellar peduncle and folia in the intermediate zone of the cerebellum. Antibody specificity was confirmed by absence of labelling in hindbrain tissue from peripherin knockout mice. This study shows that in the adult mouse hindbrain, peripherin is expressed in discrete neuronal subpopulations that have sensory, motor and autonomic functions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Beaulieu JM, Nguyen MD, Julien JP (1999) Late onset of motor neurons in mice overexpressing wild-type peripherin. J Cell Biol 147:531–544

    Article  PubMed  CAS  Google Scholar 

  • Beaulieu JM, Jacomy H, Julien JP (2000) Formation of intermediate filament protein aggregates with disparate effects in two transgenic mouse models lacking the neurofilament light subunit. J Neurosci 20:5321–5328

    PubMed  CAS  Google Scholar 

  • Beaulieu JM, Kriz J, Julien JP (2002) Induction of peripherin expression in subsets of brain neurons after lesion injury or cerebral ischemia. Brain Res 946:153–161

    Article  PubMed  CAS  Google Scholar 

  • Benson TE, Brown MC (2004) Postsynaptic targets of type II auditory nerve fibers in the cochlear nucleus. J Assoc Res Otolaryngol 5:111–125

    PubMed  Google Scholar 

  • Berglund AM, Brown MC (1994) Central trajectories of type II spiral ganglion cells from various cochlear regions in mice. Hear Res 75:121–130

    Article  PubMed  CAS  Google Scholar 

  • Berglund AM, Ryugo DK (1987) Hair cell innervation by spiral ganglion neurons in the mouse. J Comp Neurol 255:560–570

    Article  PubMed  CAS  Google Scholar 

  • Bieger D, Hopkins DA (1987) Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus. J Comp Neurol 262:546–562

    Article  PubMed  CAS  Google Scholar 

  • Brody BA, Ley CA, Parysek LM (1989) Selective distribution of the 57 kDa neural intermediate filament protein in the rat CNS. J Neurosci 9:2391–2401

    PubMed  CAS  Google Scholar 

  • Brown MC, Ledwith JV III (1990) Projections of thin (type-II) and thick (type-I) auditory-nerve fibers into the cochlear nucleus of the mouse. Hear Res 49:105–118

    Article  PubMed  CAS  Google Scholar 

  • Brown MC, Berglund AM, Kiang NY, Ryugo DK (1988) Central trajectories of type II spiral ganglion neurons. J Comp Neurol 278:581–590

    Article  PubMed  CAS  Google Scholar 

  • Chadan S, Le Gall JY, Di Giamberardino L, Filliatreau G (1994) Axonal transport of type III intermediate filament protein peripherin in intact and regenerating motor axons of the rat sciatic nerve. J Neurosci Res 39:127–139

    Article  PubMed  CAS  Google Scholar 

  • Djabali K, Portier MM, Gros F, Blobel G, Georgatos SD (1991) Network antibodies identify nuclear lamin B as a physiological attachment site for peripherin intermediate filaments. Cell 64:109–121

    Article  PubMed  CAS  Google Scholar 

  • Errante L, Tang D, Gardon M, Sekerkova G, Mugnaini E, Shaw G (1998) The intermediate filament protein peripherin is a marker for cerebellar climbing fibres. J Neurocytol 27:69–84

    Article  PubMed  CAS  Google Scholar 

  • Escurat M, Djabali K, Gumpel M, Gros F, Portier MM (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

    PubMed  CAS  Google Scholar 

  • Franklin KBJ, Paxinos G (1997) The mouse brain in stereotaxic coordinates. Academic, San Diego

    Google Scholar 

  • Gervasi C, Stewart CB, Szaro BG (2000) Xenopus laevis peripherin (XIF3) is expressed in radial glia and proliferating neural epithelial cells as well as in neurons. J Comp Neurol 423:512–531

    Article  PubMed  CAS  Google Scholar 

  • Gorham JD, Baker H, Kegler D, Ziff EB (1990) The expression of the neuronal intermediate filament protein peripherin in the rat embryo. Brain Res Dev Brain Res 57:235–248

    Article  PubMed  CAS  Google Scholar 

  • Haenggeli CA, Pongstaporn T, Doucet JR, Ryugo DK (2005) Projections from the spinal trigeminal nucleus to the cochlear nucleus in the rat. J Comp Neurol 484:191–205

    Article  PubMed  Google Scholar 

  • Hafidi A (1998) Peripherin-like immunoreactivity in type II spiral ganglion cell body and projections. Brain Res 805:181–190

    Article  PubMed  CAS  Google Scholar 

  • Helfand BT, Mendez MG, Pugh J, Delsert C, Goldman RD (2003) A role for intermediate filaments in determining and maintaining the shape of nerve cells. Mol Biol Cell 14:5069–5081

    Article  PubMed  CAS  Google Scholar 

  • Hurd LB, Hutson KA, Morest DK (1999) Cochlear nerve projections to the small cell shell of the cochlear nucleus: the neuroanatomy of extremely thin sensory axons. Synapse 33:83–117

    Article  PubMed  CAS  Google Scholar 

  • Itoh K, Kamiya H, Mitani A, Yasui Y, Takada M, Mizuno N (1987) Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat. Brain Res 400:145–150

    Article  PubMed  CAS  Google Scholar 

  • Kanjhan R, Housley GD, Burton LD, Christie DL, Kippenberger A, Thorne PR, Luo L, Ryan AF (1999) Distribution of the P2X2 receptor subunit of the ATP-gated ion channels in the rat central nervous system. J Comp Neurol 407:11–32

    Article  PubMed  CAS  Google Scholar 

  • Lariviere RC, Julien JP (2004) Functions of intermediate filaments in neuronal development and disease. J Neurobiol 58:131–148

    Article  PubMed  CAS  Google Scholar 

  • Lariviere RC, Nguyen MD, Ribeiro-da-Silva A, Julien JP (2002) Reduced number of unmyelinated sensory axons in peripherin null mice. J Neurochem 81:525–532

    Article  PubMed  CAS  Google Scholar 

  • Leonard RB, Kevetter GA (2006) Vestibular efferents contain peripherin. Neurosci Lett 408:104–107

    Article  PubMed  CAS  Google Scholar 

  • Leonard DG, Gorham JD, Cole P, Greene LA, Ziff EB (1988) A nerve growth factor-regulated messenger RNA encodes a new intermediate filament protein. J Cell Biol 106:181–193

    Article  PubMed  CAS  Google Scholar 

  • McAllen RM, Spyer KM (1976) The location of cardiac vagal preganglionic motoneurones in the medulla of the cat. J Physiol 258:187–204

    PubMed  CAS  Google Scholar 

  • Mugnaini E, Warr WB, Osen KK (1980) Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat, and mouse. J Comp Neurol 191:581–606

    Article  PubMed  CAS  Google Scholar 

  • Oblinger MM, Wong J, Parysek LM (1989) Axotomy-induced changes in the expression of a type III neuronal intermediate filament gene. J Neurosci 9:3766–3775

    PubMed  CAS  Google Scholar 

  • Parysek LM, Chisholm RL, Ley CA, Goldman RD (1988) A type III intermediate filament gene is expressed in mature neurons. Neuron 1:395–401

    Article  PubMed  CAS  Google Scholar 

  • Portier MM, de Nechaud B, Gros F (1984a) Peripherin, a new member of the intermediate filament protein family. Dev Neurosci 6:335–344

    CAS  Google Scholar 

  • Portier MM, Brachet P, Croizat B, Gros F (1984b) Regulation of peripherin in mouse neuroblastoma and rat PC 12 pheochromocytoma cell lines. Dev Neurosci 6:215–226

    CAS  Google Scholar 

  • Rhrich-Haddout F, Klosen P, Portier MM, Horvat JC (1997) Expression of peripherin, NADPH-diaphorase and NOS in the adult rat neocortex. Neuroreport 8:3313–3316

    Article  PubMed  CAS  Google Scholar 

  • Ryugo DK, Dodds LW, Benson TE, Kiang NY (1991) Unmyelinated axons of the auditory nerve in cats. J Comp Neurol 308:209–223

    Article  PubMed  CAS  Google Scholar 

  • Schimmang T, Tan J, Muller M, Zimmermann U, Rohbock K, Kopschall I, Limberger A, Minichiello L, Knipper M (2003) Lack of Bdnf and TrkB signalling in the postnatal cochlea leads to a spatial reshaping of innervation along the tonotopic axis and hearing loss. Development 130:4741–4750

    Article  PubMed  CAS  Google Scholar 

  • Shore SE, Helfert RH, Bledsoe SC Jr, Altschuler RA, Godfrey DA (1991) Descending projections to the dorsal and ventral divisions of the cochlear nucleus in guinea pig. Hear Res 52:255–268

    Article  PubMed  CAS  Google Scholar 

  • Shore SE, Vass Z, Wys NL, Altschuler RA (2000) Trigeminal ganglion innervates the auditory brainstem. J Comp Neurol 419:271–285

    Article  PubMed  CAS  Google Scholar 

  • Smith A, Gervasi C, Szaro BG (2006) Neurofilament content is correlated with branch length in developing collateral branches of Xenopus spinal cord neurons. Neurosci Lett 403:283–287

    Article  PubMed  CAS  Google Scholar 

  • Terao E, Janssens S, van den Bosch de Aguilar P, Portier M, Klosen P (2000) In vivo expression of the intermediate filament peripherin in rat motoneurons: modulation by inhibitory and stimulatory signals. Neuroscience 101:679–688

    Article  PubMed  CAS  Google Scholar 

  • Troy CM, Brown K, Greene LA, Shelanski ML (1990a) Ontogeny of the neuronal intermediate filament protein, peripherin, in the mouse embryo. Neuroscience 36:217–237

    Article  PubMed  CAS  Google Scholar 

  • Troy CM, Muma NA, Greene LA, Price DL, Shelanski ML (1990b) Regulation of peripherin and neurofilament expression in regenerating rat motor neurons. Brain Res 529:232–238

    Article  PubMed  CAS  Google Scholar 

  • Undamatla J, Szaro BG (2001) Differential expression and localization of neuronal intermediate filament proteins within newly developing neurites in dissociated cultures of Xenopus laevis embryonic spinal cord. Cell Motil Cytoskelet 49:16–32

    Article  CAS  Google Scholar 

  • Weinberg RJ, Rustioni A (1987) A cuneocochlear pathway in the rat. Neuroscience 20:209–219

    Article  PubMed  CAS  Google Scholar 

  • Wright DD, Ryugo DK (1996) Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat. J Comp Neurol 365:159–172

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S, Oka H (1998) Membrane properties of dissociated trigeminal mesencephalic neurons of the adult rat. Neurosci Res 30:227–234

    Article  PubMed  CAS  Google Scholar 

  • Yuan A, Rao MV, Sasaki T, Chen Y, Kumar A, Veeranna, Liem RK, Eyer J, Peterson AC, Julien JP, Nixon RA (2006) Alpha-internexin is structurally and functionally associated with the neurofilament triplet proteins in the mature CNS. J Neurosci 26:10006–10019

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Marsden Fund (Royal Society of New Zealand), Top Achiever Doctoral Scholarship (Tertiary Education Commission) (MB) and the James Cook Fellowship (Royal Society of New Zealand) (GH). We wish to thank Roxanne Lariviere from Laval University, Quebec, Canada for assistance with the peripherin knockout and background control tissue.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gary D. Housley.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barclay, M., Noakes, P.G., Ryan, A.F. et al. Neuronal expression of peripherin, a type III intermediate filament protein, in the mouse hindbrain. Histochem Cell Biol 128, 541–550 (2007). https://doi.org/10.1007/s00418-007-0340-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-007-0340-4

Keywords

Navigation