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Expression of the small conductance Ca2+-activated K+ channel, SK3, in the olfactory ensheathing glial cells of rat brain

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Abstract

Olfactory sensory neurons are wrapped by ensheathing glial cells in the olfactory nerve layer (ONL). Neither functional roles nor electrical properties of ensheathing glial cells have been, as yet, fully clarified. Four subunits (SK1–4) of small conductance Ca2+-activated K+ (SK) channels have been cloned. In the present study, immunohistochemical analyses showed that SK3 channels are expressed in ensheathing glial cells in the rat olfactory bulb, in addition to neuronal cells in other regions. Western blotting analysis demonstrated that SK3 was predominantly expressed in the olfactory bulb, thalamus, moderately in the hippocampus and cerebellum and modestly in the cerebral cortex of the rat brain. SK3 immunoreactivity was detected in the ONL of the olfactory bulb, neural cell body and fibers of the substantia nigra and hypothalamus. SK3 immunoreactivity was quite intense in the outer (superficial) part of the ONL. SK3-immunoreactive structures were overlapped with glial fibrillary acidic protein (GFAP), but not with vimentin, markers for glial cells and olfactory sensory axons, respectively. Immunoelectron microscopy showed that SK3 immunoreactivity was localized in thin processes that enfolded fascicles of immunonegative olfactory nerve axons. These results indicate that SK3 is expressed specifically in the olfactory ensheathing glial cells in olfactory regions.

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References

  • Au WW, Treloar HB Greer CA (2002) Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446:68–80

    Article  PubMed  Google Scholar 

  • Bliss TV, Rosenberg ME (1979) Activity-dependent changes in conduction velocity in the olfactory nerve of the tortoise. Pflügers Arch 381:209–216

    Google Scholar 

  • Burnard DM, Crichton SA, MacVicar BA (1990) Electrophysiological properties of reactive glial cells in the kainate-lesioned hippocampal slice. Brain Res 510:43–52

    Article  CAS  Google Scholar 

  • Doucette R (1993) Glial cells in the nerve fiber layer of the main olfactory bulb of embryonic and adult mammals. Microsc Res Tech 24:113–130

    CAS  PubMed  Google Scholar 

  • Eng DL, Kocsis JD (1987) Activity-dependent changes in extracellular potassium and excitability in turtle olfactory nerve. J Neurophysiol 57:740–754

    CAS  PubMed  Google Scholar 

  • Erickson KR, Ronnekleiv OK, Kelly MJ (1993) Role of a T-type calcium current in supporting a depolarizing potential, damped oscillations, and phasic firing in vasopressinergic guinea pig supraoptic neurons. Neuroendocrinology 57:789–800

    CAS  PubMed  Google Scholar 

  • Fujita A, Takeuchi T, Saitoh N, Hanai J, Hata F (2001) Expression of Ca2+-activated K+ channels, SK3, in the interstitial cells of Cajal in the gastrointestinal tract. Am J Physiol Cell Physiol 281:C1727–C1733

    CAS  PubMed  Google Scholar 

  • Gesteland RC (1986) Speculations on receptor cells as analyzers and filters. Experientia 42:287–291

    CAS  PubMed  Google Scholar 

  • Gonzalez Mde L, Malemud CJ, Silver J (1993) Role of astroglial extracellular matrix in the formation of rat olfactory bulb glomeruli. Exp Neurol 123:91–105

    Article  CAS  PubMed  Google Scholar 

  • Hibino H, Horio Y, Fujita A, Inanobe A, Doi K, Gotow T, Uchiyama Y, Kubo T, Kurachi Y (1999) Expression of an inwardly rectifying K+ channel, Kir4.1, in satellite cells of rat cochlear ganglia. Am J Physiol 277:C638–C644

    CAS  PubMed  Google Scholar 

  • Higashi K, Fujita A, Inanobe A, Tanemoto M, Doi K, Kubo T, Kurachi Y (2001) An inwardly rectifying K+ channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain. Am J Physiol Cell Physiol 281:C922–C931

    CAS  PubMed  Google Scholar 

  • Ishii TM, Silvia C, Hirschberg B, Bond CT, Adelman JP, Maylie J (1997) A human intermediate conductance calcium-activated potassium channel. Proc Natl Acad Sci USA 94:11651–11656

    CAS  PubMed  Google Scholar 

  • Jalonen TO, Margraf RR, Wielt DB, Charniga CJ, Linne ML, Kimelberg HK (1997) Serotonin induces inward potassium and calcium currents in rat cortical astrocytes. Brain Res 758:69–82

    Article  CAS  PubMed  Google Scholar 

  • Khanna R, Roy L, Zhu X, Schlichter LC (2001) K+ channels and the microglial respiratory burst. Am J Physiol Cell Physiol 280:C796–C806

    CAS  PubMed  Google Scholar 

  • Köhler M, Hirschberg B, Bond CT, Kinzie JM, Marrion NV, Maylie J, Adelman JP (1996) Small-conductance, calcium-activated potassium channels from mammalian brain. Science 273:1709–1714

    PubMed  Google Scholar 

  • Manor D, Moran N, Segal M (1994) Interactions among calcium compartments in C6 rat glioma cells: involvement of potassium channels. J Physiol 478:251–263

    CAS  PubMed  Google Scholar 

  • McCarty NA, O'Neil RG (1992) Calcium signaling in cell volume regulation. Physiol Rev 72:1037–1061

    PubMed  Google Scholar 

  • Mi H, Deerinck TJ, Ellisman MH, Schwarz TL (1995) Differential distribution of closely related potassium channels in rat Schwann cells. J Neurosci 15:3761–3774

    CAS  PubMed  Google Scholar 

  • Mi H, Deerinck TJ, Jones M, Ellisman, MH, Schwarz TL (1996) Inwardly rectifying K+ channels that may participate in K+ buffering are localized in microvilli of Schwann cells. J Neurosci 16:2421–2429

    CAS  PubMed  Google Scholar 

  • Nedergaard S, Flatman JA, Engberg I (1993) Nifedipine- and omega-conotoxin-sensitive Ca2+ conductances in guinea-pig substantia nigra pars compacta neurones. J Physiol (Lond) 466:727–747

    Google Scholar 

  • Negoescu A, Labat-Moleur F, Lorimier P, Lamarcq L, Guillermet C, Chambaz E, Brambilla E (1994) F′ab secondary antibodies: a general method for double immunolabeling with primary antisera from the same species. Efficiency control by chemiluminescence. J Histochem Cytochem 42:433–437

    CAS  PubMed  Google Scholar 

  • Price DL, Ludwig JW, Mi H, Schwarz TL, Ellisman MH (2002) Distribution of rSlo Ca2+-activated K+ channels in rat astrocyte perivascular endfeet. Brain Res 956:183–193

    Article  CAS  PubMed  Google Scholar 

  • Puro DG (1991) A calcium-activated, calcium-permeable ion channel in human retinal glial cells: modulation by basic fibroblast growth factor. Brain Res 548:329–333

    Article  CAS  PubMed  Google Scholar 

  • Ramon-Cueto A, Valverde F (1995) Olfactory bulb ensheathing glia: a unique cell type with axonal growth-promoting properties. Glia 14:163–173

    CAS  PubMed  Google Scholar 

  • Roper SD (2001) Gustatory and olfactory sensory transduction. In: Sperelakis N (ed) Cell Physiology Sourcebook, 3rd edn. Academic Press, Sandiego, pp815–831

  • Rosenbluth J (1962) The fine structure of acoustic ganglia in the rat. J Cell Biol 12:329–359

    CAS  Google Scholar 

  • Ryan AF, Schwartz IR (1983) Preferential amino acid uptake identifies type II spiral ganglion neurons in the gerbil. Hear Res 9:173–184

    Article  CAS  PubMed  Google Scholar 

  • Sah P (1996) Ca2+-activated K+ currents in neurones: types, physiological roles and modulation. Trends Neurosci 19:150–154

    Google Scholar 

  • Sailer CA, Hu H., Kaufmann WA, Trieb M, Schwarzer C, Storm JF, Knaus H-G (2002) Regional differences in distribution and functional expression of small-conductance Ca2+-activated K+ channels in rat brain. J Neurosci 22:9698–9707

    CAS  PubMed  Google Scholar 

  • Schwindt PC, Spain WJ, Crill WE (1992) Calcium-dependent potassium currents in neurons from cat sensorimotor cortex. J Neurophysiol 67:216–226

    CAS  PubMed  Google Scholar 

  • Schwob JE, Farber, NB, Gottlieb DI (1986) Neurons of the olfactory epithelium in adult rats contain vimentin. J Neurosci 6:208–217

    CAS  Google Scholar 

  • Seagar MJ, Deprez P, Martin-Moutot N, Couraud F. (1987) Detection and photoaffinity labeling of the Ca2+-activated K+ channel-associated apamin receptor in cultured astrocytes from rat brain. Brain Res 411:226–30

    Article  CAS  PubMed  Google Scholar 

  • Shepard PD, Bunney BS (1991) Repetitive firing properties of putative dopamine-containing neurons in vitro: regulation by an apamin-sensitive Ca2+-activated K+ conductance. Exp Brain Res 86:141–150

    CAS  PubMed  Google Scholar 

  • Shepherd GM, Greer CA (1998) Olfactory bulb. In: Shepherd GM (ed) The synaptic organization of the brain, 4th edn. Oxford University press, Oxford, pp159–203

  • Stocker M, Pedarzani P (2000) Differential distribution of three Ca2+-activated K+ channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system. Mol Cell Neurosci 15:476–493

    CAS  PubMed  Google Scholar 

  • Stocker M, Krause M, Pedarzani P (1999) An apamin-sensitive Ca2+-activated K+ current in hippocampal pyramidal neurons. Proc Natl Acad Sci USA 96:4662–4667

    Article  CAS  PubMed  Google Scholar 

  • Strobaek D, Jorgensen TD, Christophersen P, Ahring PK, Olesen SP (2000) Pharmacological characterization of small-conductance Ca2+-activated K+ channels stably expressed in HEK 293 cells. Br J Pharmacol 129:991–999

    CAS  PubMed  Google Scholar 

  • Valverde F, Lopez-Mascaraque L (1991) Neuroglial arrangements in the olfactory glomeruli of the hedgehog. J Comp Neurol 307:658–674

    CAS  PubMed  Google Scholar 

  • Wagner EJ, Ronnekleiv OK, Kelly MJ (2001) The noradrenergic inhibition of an apamin-sensitive, small-conductance Ca2+-activated K+ channel in hypothalamic gamma-aminobutyric acid neurons: pharmacology, estrogen sensitivity, and relevance to the control of the reproductive axis. J Pharmacol Exp Ther 299:21–30

    CAS  PubMed  Google Scholar 

  • Wolfart, J, Neuhoff, H, Franz O, Roeper J (2001) Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J Neurosci 21:3443–3456

    CAS  PubMed  Google Scholar 

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Acknowledgement

We thank Dr. G.S. Drummond (WellSpring Pharmaceutical Corporation, N.J., USA) for critical reading of this manuscript.

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Correspondence to Akikazu Fujita.

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This work was supported in part by a Grant-in-Aid to A.F. for Scientific Research from the Ministry of Education, Science, Sports and Culture of Japan, and by scholarship from Ono Pharmaceutical Company, and by Narishige Neuroscience Research Foundation.

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Fujita, A., Takeuchi, T., Hanai, J. et al. Expression of the small conductance Ca2+-activated K+ channel, SK3, in the olfactory ensheathing glial cells of rat brain. Cell Tissue Res 313, 187–193 (2003). https://doi.org/10.1007/s00441-003-0752-y

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