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Differentiation of Boettcher’s cells during postnatal development of rat cochlea

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Abstract

Contrary to the highly specialized epithelial cells of the mammalian auditory organ, little is known about the surrounding cells and, in particular, Boettcher’s cells (BC). Our morphological studies show that, in rats, these cells began their differentiation around postnatal day 8 (P8) reaching maturity around P20, when they are completely covered by Hensen’s and Claudius’ cells. Tight junctions were noted near the apex of BC, providing that they were in direct contact with the endolymphatic space, between approximately P8 and P16. We observed gap junctions between BC and adjacent cells before the end of the covering process suggesting the additional involvement of BC in potassium recycling into the endolymph. Adherens junctions were also seen between BC throughout their maturation. Importantly, we noticed cytoplasmic secretory granules and an accumulated material, probably a secretion, in the intercellular space, between P8 and P25. These results indicate that BC could basally take part in the secretion of the extracellular matrix of the basilar membrane. Finally, we show that the basolateral interdigitations of BC are longer and more tighlty grouped at maturity and harbour urea transporters as early as P18. Our observations thus support the view that BC perform several functions.

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Abbreviations

BC:

Boettcher’s cells

CC:

Claudius’ cells

Cx26:

Connexin 26

HeC:

Hensen’s cells

P:

Postnatal

UT-B:

Urea transporter-B

References

  • Abe T, Kakehata S, Kitani R, Maruya S, Navaratnam D, Santos-Sacchi J, Shinkawa H (2007) Developmental expression of the outer hair cell motor prestin in the mouse. J Membr Biol 215:49–56

    Article  PubMed  CAS  Google Scholar 

  • Crispino G, Di Pasquale G, Scimemi P, Rodriguez L, Galindo Ramirez F, De Siati RD, Santarelli RM, Arslan E, Bortolozzi M, Chiorini JA, Mammano F (2011) BAAV mediated GJB2 gene transfer restores gap junction coupling in cochlear organotypic cultures from deaf Cx26Sox10Cre mice. PLoS One 6:e23279

    Article  PubMed  CAS  Google Scholar 

  • Hibino H, Horio Y, Inanobe A, Doi K, Ito M, Yamada M, Gotow T, Uchiyama Y, Kawamura M, Kubo T, Kurachi Y (1997) An ATP-dependent inwardly rectifying potassium channel, KAB-2 (Kir4. 1), in cochlear stria vascularis of inner ear: its specific subcellular localization and correlation with the formation of endocochlear potential. J Neurosci 17:4711–4721

    PubMed  CAS  Google Scholar 

  • Hibino H, Nin F, Tsuzuki C, Kurachi Y (2010) How is the highly positive endocochlear potential formed? The specific architecture of the stria vascularis and the roles of the ion-transport apparatus. Pflugers Arch 459:521–533

    Article  PubMed  CAS  Google Scholar 

  • Hirt B, Penkova ZH, Eckhard A, Liu W, Rask-Andersen H, Muller M, Lowenheim H (2010) The subcellular distribution of aquaporin 5 in the cochlea reveals a water shunt at the perilymph-endolymph barrier. Neuroscience 168:957–970

    Article  PubMed  CAS  Google Scholar 

  • Ishiyama E, Cutt RA, Keels EW (1970) Distribution and ultrastructure of the Boettcher’s cells in mammals. Ann Otol Rhinol Laryngol 79:54–69

    PubMed  CAS  Google Scholar 

  • Jahnke K (1975) The fine structure of freeze-fractured intercellular junctions in the guinea pig inner ear. Acta Otolaryngol Suppl 336:1–40

    PubMed  CAS  Google Scholar 

  • Johnen N, Francart M-E, Thelen N, Cloes M, Thiry M (2012) Evidence for a partial epithelial–mesenchymal transition in postnatal stages of rat auditory organ morphogenesis. Histochem Cell Biol 138:477–488

    Article  PubMed  CAS  Google Scholar 

  • Kanazawa A, Sunami K, Takayama M, Nishiura H, Tokuhara Y, Sakamoto H, Iguchi H, Yamane H (2004) Probable function of Boettcher cells based on results of morphological study: localization of nitric oxide synthase. Acta Otolaryngol Suppl 554:12–16

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi T, Kimura RS, Paul DL, Adams JC (1995) Gap junctions in the rat cochlea: immunohistochemical and ultrastructural analysis. Anat Embryol 191:101–118

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi T, Adams JC, Miyabe Y, So E, Kobayashi T (2000) Potassium ion recycling pathway via gap junction systems in the mammalian cochlea and its interruption in hereditary nonsyndromic deafness. Med Electron Microsc 33:51–56

    Article  PubMed  CAS  Google Scholar 

  • Kitajiri S-i, Furuse M, Morita K, Saishin-Kiuchi Y, Kido H, Ito J, Tsukita S (2004) Expression patterns of claudins, tight junction adhesion molecules, in the inner ear. Hear Res 187:25–34

    Article  PubMed  CAS  Google Scholar 

  • Kwun YS, Yeo SW, Ahn YH, Lim SW, Jung JY, Kim WY, Sands JM, Kim J (2003) Immunohistochemical localization of urea transporters A and B in the rat cochlea. Hear Res 183:84–96

    Article  PubMed  CAS  Google Scholar 

  • Lang F, Vallon V, Knipper M, Wangemann P (2007) Functional significance of channels and transporters expressed in the inner ear and kidney. Am J Physiol Cell Physiol 293:C1187–C1208

    Article  PubMed  CAS  Google Scholar 

  • Lange K (2011) Fundamental role of microvilli in the main functions of differentiated cells: outline of an universal regulating and signaling system at the cell periphery. J Cell Physiol 226:896–927

    Article  PubMed  CAS  Google Scholar 

  • Marcotti W, Johnson SL, Holley MC, Kros CJ (2003) Developmental changes in the expression of potassium currents of embryonic, neonatal and mature mouse inner hair cells. J Physiol (Lond) 548:383–400

    Article  CAS  Google Scholar 

  • Merchan MA, Merchan JA, Ludena MD (1980) Morphology of Hensen’s cells. J Anat 131:519–523

    PubMed  CAS  Google Scholar 

  • Montcouquiol M, Kelley MW (2003) Planar and vertical signals control cellular differentiation and patterning in the mammalian cochlea. J Neurosci 23:9469–9478

    PubMed  CAS  Google Scholar 

  • Nakazawa K (2001) Ultrastructural localization of calmodulin in gerbil cochlea by immunogold electron microscopy. Hear Res 151:133–140

    Article  PubMed  CAS  Google Scholar 

  • Okamura H-o, Sugai N, Suzuki K, Ohtani I (1996) Enzyme-histochemical localization of carbonic anhydrase in the inner ear of the guinea pig and several improvements of the technique. Histochem Cell Biol 106:425–430

    Article  PubMed  CAS  Google Scholar 

  • Ramprashad F, Money KE, Landolt JP, Correia MJ, Laufer J (1983) Distribution and size of Boettcher cells in the little brown bat, rabbit, and other species. Anat Rec 207:653–663

    Article  PubMed  CAS  Google Scholar 

  • Roth B, Bruns V (1992) Postnatal development of the rat organ of Corti. I. General morphology, basilar membrane, tectorial membrane and border cells. Anat Embryol 185:559–569

    Article  PubMed  CAS  Google Scholar 

  • Santi PA, Larson JT, Furcht LT, Economou TS (1989) Immunohistochemical localization of fibronectin in the chinchilla cochlea. Hear Res 39:91–101

    Article  PubMed  CAS  Google Scholar 

  • Schulte BA, Steel KP (1994) Expression of alpha and beta subunit isoforms of Na,K-ATPase in the mouse inner ear and changes with mutations at the Wv or Sld loci. Hear Res 78:65–76

    Article  PubMed  CAS  Google Scholar 

  • Spicer SS, Schulte BA (1994) Ultrastructural differentiation of the first Hensen cell in the gerbil cochlea as a distinct cell type. Anat Rec 240:149–156

    Article  PubMed  CAS  Google Scholar 

  • Spicer SS, Smythe N, Schulte BA (2003) Ultrastructure indicative of ion transport in tectal, Deiters, and tunnel cells: differences between gerbil and chinchilla basal and apical cochlea. Anat Rec A Discov Mol Cell Evol Biol 271:342–359

    Article  PubMed  Google Scholar 

  • Thelen N, Breuskin I, Malgrange B, Thiry M (2009) Early identification of inner pillar cells during rat cochlear development. Cell Tissue Res 337:1–14

    Article  PubMed  CAS  Google Scholar 

  • Timmer RT, Klein JD, Bagnasco SM, Doran JJ, Verlander JW, Gunn RB, Sands JM (2001) Localization of the urea transporter UT-B protein in human and rat erythrocytes and tissues. Am J Physiol Cell Physiol 281:C1318–C1325

    PubMed  CAS  Google Scholar 

  • Wang XH, Streeter M, Liu YP, Zhao HB (2009) Identification and characterization of pannexin expression in the mammalian cochlea. J Comp Neurol 512:336–346

    Article  PubMed  CAS  Google Scholar 

  • Welsch U, Riedelsheimer B (1997) Histophysiological observations on the external auditory meatus, middle, and inner ear of the Weddell seal (Leptonychotes weddelli). J Morphol 234:25–36

    Article  PubMed  CAS  Google Scholar 

  • Wu L, Sagong B, Choi JY, Kim UK, Bok J (2013) A systematic survey of carbonic anhydrase mRNA expression during mammalian inner ear development. Dev Dyn 242:269–280

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. J. Sands (Emory University School of Medicine, Atlanta, USA) for providing the UT-B antibody and Mrs P. Piscicelli for her skillful technical assistance. We also thank the GIGA-Imaging and Flow Cytometry Platform (University of Liege) for allowing us to use their laser-scanning confocal-microscopy equipment and for their technical support.

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Authors and Affiliations

  1. Unit of Cell Biology, GIGA-Neurosciences, University of Liege, CHU Sart-Tilman, B36, 4000, Liege, Belgium

    Marie Cloes, Thomas Renson, Nicolas Johnen, Nicolas Thelen & Marc Thiry

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  1. Marie Cloes
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  2. Thomas Renson
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  3. Nicolas Johnen
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  4. Nicolas Thelen
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  5. Marc Thiry
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Corresponding authors

Correspondence to Marie Cloes or Marc Thiry.

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The authors declare no conflicts of interest.

This work received financial support from the F.R.S.-FNRS (grant no. 3.4551.10). M.C. is a F.R.S.-FNRS Research Fellow. N.J. is a PhD grant holder of the FRIA.

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Cloes, M., Renson, T., Johnen, N. et al. Differentiation of Boettcher’s cells during postnatal development of rat cochlea. Cell Tissue Res 354, 707–716 (2013). https://doi.org/10.1007/s00441-013-1705-8

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