Freshly dissociated mature hippocampal astrocytes exhibit passive membrane conductance and low membrane resistance similarly to syncytial coupled astrocytes

Journal of Neurophysiology

Volumn 113, Issue 10, 2015, Pages 3744-3750

  Du, Yixing ^a,b   Ma, Baofeng ^a   Kiyoshi, Conrad M ^a   Alford, Catherine C ^a   Wang, Wei ^a,c   Zhou, Min ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Astrocytes; Hippocampus; Membrane resistance; Passive membrane conductance; Patch clamp recording

Indexed keywords

POTASSIUM CHANNEL; POTASSIUM; RHODAMINE; SULFORHODAMINE 101;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN SLICE; CELL MATURATION; CELL SELECTION; CELL STRUCTURE; CELL SUSPENSION; CONTROLLED STUDY; FEMALE; GAP JUNCTION; HIPPOCAMPAL ASTROCYTE; HIPPOCAMPUS; HYPERPOLARIZATION; MALE; MEMBRANE CONDUCTANCE; MEMBRANE CURRENT; MEMBRANE RESISTANCE; MEMBRANE STEADY POTENTIAL; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NEUROTRANSMITTER UPTAKE; NONHUMAN; OLFACTORY ENSHEATHING CELL; POTASSIUM CELL LEVEL; PRIORITY JOURNAL; REVERSAL POTENTIAL; SYNCYTIAL COUPLED ASTROCYTE; WHOLE CELL PATCH CLAMP; YOUNG ADULT; ANIMAL; BIOPHYSICS; CONFOCAL MICROSCOPY; CYTOLOGY; ELECTROSTIMULATION; IN VITRO STUDY; MEMBRANE POTENTIAL; METABOLISM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY;

ANIMALS; ASTROCYTES; BIOPHYSICS; ELECTRIC STIMULATION; GAP JUNCTIONS; HIPPOCAMPUS; IN VITRO TECHNIQUES; MEMBRANE POTENTIALS; MICE; MICROSCOPY, CONFOCAL; PATCH-CLAMP TECHNIQUES; POTASSIUM; RHODAMINES;

EID: 84931281972     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00206.2015     Document Type: Article

References (40)

1. Benedikt J, Inyushin M, Kucheryavykh YV, Rivera Y, Kucheryavykh LY, Nichols CG, Eaton MJ, Skatchkov SN. Intracellular polyamines enhance astrocytic coupling. Neuroreport 23: 1021–1025, 2012.
2. Berger T, Schnitzer J, Kettenmann H. Developmental changes in the membrane current pattern, K+ buffer capacity, and morphology of glial cells in the corpus callosum slice. J Neurosci 11: 3008–3024, 1991.
3. Bushong EA, Martone ME, Jones YZ, Ellisman MH. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22: 183–192, 2002.
4. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28: 264–278, 2008.
5. Chever O, Djukic B, McCarthy KD, Amzica F. Implication of Kir4.1 channel in excess potassium clearance: an in vivo study on anesthetized glial-conditional Kir4.1 knock-out mice. J Neurosci 30: 15769–15777, 2010.
6. Chu KC, Chiu CD, Hsu TT, Hsieh YM, Huang YY, Lien CC. Functional identification of an outwardly rectifying pH- and anesthetic-sensitive leak K+ conductance in hippocampal astrocytes. Eur J Neurosci 32: 725–735, 2010.
7. Djukic B, Casper KB, Philpot BD, Chin LS, McCarthy KD. Conditional knock-out of Kir4.1 leads to glial membrane depolarization, inhibition of potassium and glutamate uptake, and enhanced short-term synaptic potentiation. J Neurosci 27: 11354–11365, 2007.
8. Han X, Chen M, Wang F, Windrem M, Wang S, Shanz S, Xu Q, Oberheim NA, Bekar L, Betstadt S, Silva AJ, Takano T, Goldman SA, Nedergaard M. Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell 12: 342–353, 2013.
9. Haseleu J, Anlauf E, Blaess S, Endl E, Derouiche A. Studying subcellular detail in fixed astrocytes: dissociation of morphologically intact glial cells (DIMIGs). Front Cell Neurosci 7: 54, 2013.
10. Hille B. Ion Channels of Excitable Cells. Sunderland, MA: Sinauer, 2001.
11. Hwang EM, Kim E, Yarishkin O, Woo DH, Han KS, Park N, Bae Y, Woo J, Kim D, Park M, Lee CJ, Park JY. A disulphide-linked heterodimer of TWIK-1 and TREK-1 mediates passive conductance in astrocytes. Nat Commun 5: 3227, 2014.
12. Kafitz KW, Meier SD, Stephan J, Rose CR. Developmental profile and properties of sulforhodamine 101-labeled glial cells in acute brain slices of rat hippocampus. J Neurosci Methods 169: 84–92, 2008.
13. Kimelberg HK, Cai Z, Schools G, Zhou M. Acutely isolated astrocytes as models to probe astrocyte functions. Neurochem Int 36: 359–367, 2000.
14. Kucheryavykh YV, Kucheryavykh LY, Nichols CG, Maldonado HM, Baksi K, Reichenbach A, Skatchkov SN, Eaton MJ. Downregulation of Kir4.1 inward rectifying potassium channel subunits by RNAi impairs potassium transfer and glutamate uptake by cultured cortical astrocytes. Glia 55: 274–281, 2007.
15. Kucheryavykh YV, Shuba YM, Antonov SM, Inyushin MY, Cubano L, Pearson WL, Kurata H, Reichenbach A, Veh RW, Nichols CG, Eaton MJ, Skatchkov SN. Complex rectification of Muller cell Kir currents. Glia 56: 775–790, 2008.
16. Kuffler SW, Nicholls JG, Orkand RK. Physiological properties of glial cells in the central nervous system of amphibia. J Neurophysiol 29: 768–787, 1966.
17. Laube G, Veh RW. Astrocytes, not neurons, show most prominent staining for spermidine/spermine-like immunoreactivity in adult rat brain. Glia 19: 171–179, 1997.
18. Liu X, Bolteus AJ, Balkin DM, Henschel O, Bordey A. GFAP-expressing cells in the postnatal subventricular zone display a unique glial phenotype intermediate between radial glia and astrocytes. Glia 54: 394–410, 2006.
19. Longden TA, Dunn KM, Draheim HJ, Nelson MT, Weston AH, Edwards G. Intermediate-conductance calcium-activated potassium channels participate in neurovascular coupling. Br J Pharmacol 164: 922–933, 2011.
20. Ma B, Xu G, Wang W, Enyeart JJ, Zhou M. Dual patch voltage clamp study of low membrane resistance astrocytes in situ. Mol Brain 7: 18, 2014.
21. Nimmerjahn A, Kirchhoff F, Kerr JN, Helmchen F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 1: 31–37, 2004.
22. Olsen ML, Sontheimer H. Functional implications for Kir4.1 channels in glial biology: from K+ buffering to cell differentiation. J Neurochem 107: 589–601, 2008.
23. Orkand RK, Nicholls JG, Kuffler SW. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol 29: 788–806, 1966.
24. Park H, Han KS, Oh SJ, Jo S, Woo J, Yoon BE, Lee CJ. High glutamate permeability and distal localization of Best1 channel in CA1 hippocampal astrocyte. Mol Brain 6: 54, 2013.
25. Rela L, Bordey A, Greer CA. Olfactory ensheathing cell membrane properties are shaped by connectivity. Glia 58: 665–678, 2010.
26. Schoos GP, Zhou M, Kimelberg HK. Development of gap junctions in hippocampal astrocytes: evidence that whole cell electrophysiological phenotype is an intrinsic property of the individual cell. J Neurophysiol 96: 1383–1392, 2006.
27. Schroder W, Hinterkeuser S, Seifert G, Schramm J, Jabs R, Wilkin GP, Steinhauser C. Functional and molecular properties of human astrocytes in acute hippocampal slices obtained from patients with temporal lobe epilepsy. Epilepsia 41, Suppl 6: S181–S184, 2000.
28. Seifert G, Huttmann K, Binder DK, Hartmann C, Wyczynski A, Neusch C, Steinhauser C. Analysis of astroglial K+ channel expression in the developing hippocampus reveals a predominant role of the Kir4.1 subunit. J Neurosci 29: 7474–7488, 2009.
29. Skatchkov SN, Eaton MJ, Krusek J, Veh RW, Biedermann B, Bringmann A, Pannicke T, Orkand RK, Reichenbach A. Spatial distribution of spermine/spermidine content and K+-current rectification in frog retinal glial (Muller) cells. Glia 31: 84–90, 2000.
30. Skatchkov SN, Eaton MJ, Shuba YM, Kucheryavykh YV, Derst C, Veh RW, Wurm A, Iandiev I, Pannicke T, Bringmann A, Reichenbach A. Tandem-pore domain potassium channels are functionally expressed in retinal (Muller) glial cells. Glia 53: 266–276, 2006.
31. Steinhauser C, Berger T, Frotscher M, Kettenmann H. Heterogeneity in the membrane current pattern of identified glial cells in the hippocampal slice. Eur J Neurosci 4: 472–484, 1992.
32. Stephan J, Haack N, Kafitz KW, Durry S, Koch D, Hochstrate P, Seifert G, Steinhauser C, Rose CR. Kir4.1 channels mediate a depolarization of hippocampal astrocytes under hyperammonemic conditions in situ. Glia 60: 965–978, 2012.
33. Sun W, McConnell E, Pare JF, Xu Q, Chen M, Peng W, Lovatt D, Han X, Smith Y, Nedergaard M. Glutamate-dependent neuroglial calcium signaling differs between young and adult brain. Science 339: 197–200, 2013.
34. Tong X, Ao Y, Faas GC, Nwaobi SE, Xu J, Haustein MD, Anderson MA, Mody I, Olsen ML, Sofroniew MV, Khakh BS. Astrocyte Kir4.1 ion channel deficits contribute to neuronal dysfunction in Huntington’s disease model mice. Nat Neurosci 17: 694–703, 2014.
35. Wallraff A, Kohling R, Heinemann U, Theis M, Willecke K, Steinhauser C. The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J Neurosci 26: 5438–5447, 2006.
36. Walz W. Controversy surrounding the existence of discrete functional classes of astrocytes in adult gray matter. Glia 31: 95–103, 2000.
37. Wang W, Putra A, Schools GP, Ma B, Chen H, Kaczmarek LK, Barhanin J, Lesage F, Zhou M. The contribution of TWIK-1 channels to astrocyte K+ current is limited by retention in intracellular compartments. Front Cell Neurosci 7: 246, 2013.
38. Zayas-Santiago A, Agte S, Rivera Y, Benedikt J, Ulbricht E, Karl A, Davila J, Savvinov A, Kucheryavykh Y, Inyushin M, Cubano LA, Pannicke T, Veh RW, Francke M, Verkhratsky A, Eaton MJ, Reichenbach A, Skatchkov SN. Unidirectional photoreceptor-to-Muller glia coupling and unique K+ channel expression in Caiman retina. PLoS One 9: e97155, 2014.
39. Zhou M, Schools GP, Kimelberg HK. Development of GLAST(+) astrocytes and NG2(+) glia in rat hippocampus CA1: mature astrocytes are electrophysiologically passive. J Neurophysiol 95: 134–143, 2006.
40. Zhou M, Xu G, Xie M, Zhang X, Schoos GP, Ma L, Kimelberg HK, Chen H. TWIK-1 and TREK-1 are potassium channels contributing significantly to astrocyte passive conductance in rat hippocampal slices. J Neurosci 29: 8551–8564, 2009.