Skip to main content

Advertisement

Log in

Roles of gap junctions in glucose transport from glucose transporter 1-positive to -negative cells in the lateral wall of the rat cochlea

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

Abstract

Despite the importance of glucose metabolism for auditory function, the mechanisms of glucose transport in the cochlea are not completely understood. We hypothesized that gap junctions mediate intercellular glucose transport in the cochlea in cooperation with facilitative glucose transporter 1 (GLUT1). Immunohistochemistry showed that GLUT1 and the tight junction protein occludin were expressed in blood vessels, and GLUT1, the gap junction proteins connexin26 and connexin30, and occludin were also present in strial basal cells in the lateral wall of the rat cochlea. Gap junctions were found among not only these GLUT1-positive strial basal cells but also GLUT1-negative fibrocytes in the spiral ligaments and strial intermediate cells. Glucose imaging using 6-[N-(7-nitrobenz-2-oxa-1,3-diazol-4-yl)amino]-6-deoxyglucose (6-NBDG, MW 342) together with Evans Blue Albumin (EBA, MW 68,000) showed that 6-NBDG was rapidly distributed throughout the stria vascularis and spiral ligament, whereas EBA was localized only in the vessels. The gap junctional uncouplers heptanol and carbenoxolone inhibited the distribution of 6-NBDG in the spiral ligament without decreasing the fluorescence of EBA in the blood vessels. These findings suggest that gap junctions mediate glucose transport from GLUT1-positive cells (strial basal cells) to GLUT1-negative cells (fibrocytes in the spiral ligament and strial intermediate cells) in the cochlea.

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
Fig. 7

Similar content being viewed by others

References

  • Anderson JM, Van Itallie CM (1999) Tight junctions: closing in on the seal. Curr Biol 9:R922–R924

    Article  PubMed  CAS  Google Scholar 

  • Ando M, Edamatsu M, Fukuizumi S, Takeuchi S (2008) Cellular localization of facilitated glucose transporter 1 (GLUT-1) in the cochlear stria vascularis: its possible contribution to the transcellular glucose pathway. Cell Tissue Res 331:763–769

    Article  PubMed  CAS  Google Scholar 

  • Beyer EC, Paul DL, Goodenough DA (1990) Connexin family of gap junction proteins. J Membr Biol 116:187–194

    Article  PubMed  CAS  Google Scholar 

  • Farrell CL, Pardridge WM (1991) Blood–brain barrier glucose transporter is asymmetrically distributed on brain capillary endothelial lumenal and ablumenal membranes: an electron microscopic immunogold study. Proc Natl Acad Sci USA 88:5779–5783

    Article  PubMed  CAS  Google Scholar 

  • Florian P, Amasheh S, Lessidrensky M, Todt I, Bloedow A, Ernst A, Fromm M, Gitter AH (2003) Claudins in the tight junctions of stria vascularis marginal cells. Biochem Biophys Res Commun 304:5–10

    Article  PubMed  CAS  Google Scholar 

  • Forge A (1984) Gap junctions in the stria vascularis and effects of ethacrynic acid. Hear Res 13:189–200

    Article  PubMed  CAS  Google Scholar 

  • Gabriel HD, Jung D, Butzler C, Temme A, Traub O, Winterhager E, Willecke K (1998) Transplacental uptake of glucose is decreased in embryonic lethal connexin26-deficient mice. J Cell Biol 140:1453–1461

    Article  PubMed  CAS  Google Scholar 

  • Giaume C, Tabernero A, Medina JM (1997) Metabolic trafficking through astrocytic gap junctions. Glia 21:114–123

    Article  PubMed  CAS  Google Scholar 

  • Grifa A, Wagner CA, D’Ambrosio L, Melchionda S, Bernardi F, Lopez-Bigas N, Rabionet R, Arbones M, Monica MD, Estivill X, Zelante L, Lang F, Gasparini P (1999) Mutations in GJB6 cause nonsyndromic autosomal dominant deafness at DFNA3 locus. Nat Genet 23:16–18

    PubMed  CAS  Google Scholar 

  • Ito M, Spicer SS, Schulte BA (1993) Immunohistochemical localization of brain type glucose transporter in mammalian inner ears: comparison of developmental and adult stages. Hear Res 71:230–238

    Article  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 

  • Kelsell DP, Dunlop J, Stevens HP, Lench NJ, Liang JN, Parry G, Mueller RF, Leigh IM (1997) Connexin 26 mutations in hereditary non-syndromic sensorineural deafness. Nature 387:80–83

    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 (Berl) 191:101–118

    CAS  Google Scholar 

  • Kikuchi T, Kimura RS, Paul DL, Takasaka T, Adams JC (2000) Gap junction systems in the mammalian cochlea. Brain Res Rev 32:163–166

    Article  PubMed  CAS  Google Scholar 

  • Kitajiri SI, 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 

  • Lautermann J, ten Cate WJ, Altenhoff P, Grummer R, Traub O, Frank H, Jahnke K, Winterhager E (1998) Expression of the gap-junction connexins 26 and 30 in the rat cochlea. Cell Tissue Res 294:415–420

    Article  PubMed  CAS  Google Scholar 

  • Liu XZ, Xia XJ, Xu LR, Pandya A, Liang CY, Blanton SH, Brown SD, Steel KP, Nance WE (2000) Mutations in connexin31 underlie recessive as well as dominant non-syndromic hearing loss. Hum Mol Genet 9:63–67

    Article  PubMed  CAS  Google Scholar 

  • Matsunami T, Suzuki T, Hisa Y, Takata K, Takamatsu T, Oyamada M (2006) Gap junctions mediate glucose transport between GLUT1-positive and -negative cells in the spiral limbus of the rat cochlea. Cell Commun Adhes 13:93–102

    Article  PubMed  CAS  Google Scholar 

  • Nadol JB Jr, Mulroy MJ, Goodenough DA, Weiss TF (1976) Tight and gap junctions in a vertebrate inner ear. Am J Anat 147:281–301

    Article  PubMed  Google Scholar 

  • Nakazawa K, Spicer SS, Gratton MA, Schulte BA (1996) Localization of actin in basal cells of stria vascularis. Hear Res 96:13–19

    Article  PubMed  CAS  Google Scholar 

  • Reale E, Luciano L, Franke K, Pannese E, Wermbter G, Iurato S (1975) Intercellular junctions in the vascular stria and spiral ligament. J Ultrastruct Res 53:284–297

    Article  PubMed  CAS  Google Scholar 

  • Rozental R, Srinivas M, Spray DC (2001) How to close a gap junction channel. Efficacies and potencies of uncoupling agents. Methods Mol Biol 154:447–476

    PubMed  CAS  Google Scholar 

  • Ryan AF (2001) Circulation of the inner ear: II. The relationship between metabolism and blood flow in the cochlea. In: Janh A, Santos-Sacchi J (eds) Physiology of the ear. vol. Singular, San Diego, pp 321–331

    Google Scholar 

  • Ryan AF, Goodwin P, Woolf NK, Sharp F (1982) Auditory stimulation alters the pattern of 2-deoxyglucose uptake in the inner ear. Brain Res 234:213–225

    Article  PubMed  CAS  Google Scholar 

  • Shin BC, Suzuki T, Tanaka S, Kuraoka A, Shibata Y, Takata K (1996) Connexin 43 and the glucose transporter, GLUT1, in the ciliary body of the rat. Histochem Cell Biol 106:209–214

    Article  PubMed  CAS  Google Scholar 

  • Sohl G, Willecke K (2003) An Update on Connexin Genes and their Nomenclature in Mouse and Man. Cell Commun Adhes 10:173–180

    Article  PubMed  Google Scholar 

  • Spicer SS, Schulte BA (1996) The fine structure of spiral ligament cells relates to ion return to the stria and varies with place-frequency. Hear Res 100:80–100

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Oyamada M, Takamatsu T (2001) Different regulation of connexin26 and ZO–1 in cochleas of developing rats and of guinea pigs with endolymphatic hydrops. J Histochem Cytochem 49:573–586

    PubMed  CAS  Google Scholar 

  • Suzuki T, Takamatsu T, Oyamada M (2003) Expression of gap junction protein connexin43 in the adult rat cochlea. Comparison with connexin26. J Histochem Cytochem 51:903–912

    PubMed  CAS  Google Scholar 

  • Takata K, Hirano H (1997) Mechanism of glucose transport across the human and rat placental barrier: a review. Microsc Res Tech 38:145–152

    Article  PubMed  CAS  Google Scholar 

  • Takata K, Hirano H, Kasahara M (1997) Transport of glucose across the blood-tissue barriers. Int Rev Cytol 172:1–53

    Article  PubMed  CAS  Google Scholar 

  • Tserentsoodol N, Shin BC, Suzuki T, Takata K (1998) Colocalization of tight junction proteins, occludin and ZO–1, and glucose transporter GLUT1 in cells of the blood-ocular barrier in the mouse eye. Histochem Cell Biol 110:543–551

    Article  PubMed  CAS  Google Scholar 

  • Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2:285–293

    Article  PubMed  CAS  Google Scholar 

  • Vorbrodt AW, Dobrogowska DH, Tarnawski M (2001) Immunogold study of interendothelial junction-associated and glucose transporter proteins during postnatal maturation of the mouse blood-brain barrier. J Neurocytol 30:705–716

    Article  PubMed  CAS  Google Scholar 

  • Wangemann P, Schacht J (1996) Homeostatic mechanisms in the cochlea. In: Dallos P, Popper AN, Fay R (eds) the cochlea vol. Springer-Verlag, New York, pp 130–185

    Google Scholar 

  • Wilcox ER, Burton QL, Naz S, Riazuddin S, Smith TN, Ploplis B, Belyantseva I, Ben-Yosef T, Liburd NA, Morell RJ, Kachar B, Wu DK, Griffith AJ, Friedman TB (2001) Mutations in the gene encoding tight junction claudin–14 cause autosomal recessive deafness DFNB29. Cell 104:165–172

    Article  PubMed  CAS  Google Scholar 

  • Wood IS, Trayhurn P (2003) Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. Br J Nutr 89:3–9

    Article  PubMed  CAS  Google Scholar 

  • Xia JH, Liu CY, Tang BS, Pan Q, Huang L, Dai HP, Zhang BR, Xie W, Hu DX, Zheng D, Shi XL, Wang DA, Xia K, Yu KP, Liao XD, Feng Y, Yang YF, Xiao JY, Xie DH, Huang JZ (1998) Mutations in the gene encoding gap junction protein beta-3 associated with autosomal dominant hearing impairment. Nat Genet 20:370–373 (published erratum appears in Nat Genet 21 (1999) 241)

    Article  PubMed  CAS  Google Scholar 

  • Xia AP, Ikeda K, Katori Y, Oshima T, Kikuchi T, Takasaka T (2000) Expression of connexin 31 in the developing mouse cochlea. NeuroReport 11:2449–2453

    Article  PubMed  CAS  Google Scholar 

  • Yoshihara T, Satoh M, Yamamura Y, Itoh H, Ishii T (1999) Ultrastructural localization of glucose transporter 1 (GLUT1) in guinea pig stria vascularis and vestibular dark cell areas: an immunogold study. Acta Otolaryngol 119:336–340

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Mrs. Ramona Ratliff for advice on English usage. This work was supported by grants-in-aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology, Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masahito Oyamada.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suzuki, T., Matsunami, T., Hisa, Y. et al. Roles of gap junctions in glucose transport from glucose transporter 1-positive to -negative cells in the lateral wall of the rat cochlea. Histochem Cell Biol 131, 89–102 (2009). https://doi.org/10.1007/s00418-008-0502-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-008-0502-z

Keywords

Navigation