Astrocytes in the retrotrapezoid nucleus sense H+ by inhibition of a Kir4.1-Kir5.1-like current and may contribute to chemoreception by a purinergic mechanism

Journal of Neurophysiology

Volumn 104, Issue 6, 2010, Pages 3042-3052

  Wenker, Ian C ^a   Kréneisz, Orsolya ^a   Nishiyama, Akiko ^a   Mulkey, Daniel K ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALDEHYDE DEHYDROGENASE 1L1; BARIUM ION; BICARBONATE; CARBON DIOXIDE; DESIPRAMINE; FLUOROCITRIC ACID; POTASSIUM CHANNEL; POTASSIUM CHANNEL KIR4.1; POTASSIUM CHANNEL KIR5.1; PROTON; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN REGION; BRAIN SLICE; CHEMORECEPTOR; CONTROLLED STUDY; CYTOPLASM; ELECTROPHYSIOLOGY; GLIA CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NERVE CELL; NEWBORN; NONHUMAN; PATCH CLAMP; PH MEASUREMENT; PRIORITY JOURNAL; RAT; RETROTRAPEZOID NUCLEUS; SENSITIVITY ANALYSIS;

EID: 78650915227     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00544.2010     Document Type: Article

References (45)

1. Abbott SB, Stornetta RL, Fortuna MG, DePuy SD, West GH, Harris TE, Guyenet PG. Photostimulation of retrotrapezoid nucleus phox2b-expressing neurons in vivo produces long-lasting activation of breathing in rats. J Neurosci 29: 5806-5819, 2009.
2. Bayliss DA, Talley EM, Sirois JE, Lei Q. TASK-1 is a highly modulated pH-sensitive "leak" K(+) channel expressed in brainstem respiratory neurons. Respir Physiol 129: 159-174, 2001.
3. 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.
4. Casamassima M, D'Adamo MC, Pessia M, Tucker SJ. Identification of a heteromeric interaction that influences the rectification, gating, and pH sensitivity of Kir4.1/Kir5.1 potassium channels. J Biol Chem 278: 43533-43540, 2003.
5. Chesler M. Regulation and modulation of pH in the brain. Physiol Rev 83: 1183-1221, 2003.
6. Deitmer JW. Electrogenic sodium-dependent bicarbonate secretion by glial cells of the leech central nervous system. J Gen Physiol 98: 637-655, 1991.
7. 2 chemoreception and respiratory control. J Appl Physiol 108: 1803-1811, 2010.
8. Erlichman JS, Li A, Nattie EE. Ventilatory effects of glial dysfunction in a rat brain stem chemoreceptor region. J Appl Physiol 85: 1599-1604, 1998.
9. Fellin T, Pascual O, Haydon PG. Astrocytes coordinate synaptic networks: Balanced excitation and inhibition. Physiology 21: 208-215, 2006.
10. 2+ channels. Am J Physiol Cell Physiol 284: C145-C155, 2003.
11. + on the membrane potential of silent cells in the ventral and dorsal surface layers of the rat medulla in vitro. Pflügers Arch 376: 229-235, 1978.
12. Goldstein SAN, Bayliss DA, Kim D, Lesage F, Plant LD, Rajan S. International Union of Pharmacology. LV. Nomenclature and molecular relationships of two-P potassium channels. Pharmacol Rev 57: 527-540, 2005.
13. Gordon GR, Iremonger KJ, Kantevari S, Ellis-Davies GC, MacVicar BA, Bains JS. Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. Neuron 64: 391-403, 2009.
14. Gourine AV, Kasymov V, Marina N, Tang F, Figueiredo MF, Lane S, Teschemacher AG, Spyer MK, Deisseroth K, Kasparov S. Astrocytes control breathing through pH-dependent release of ATP. Science 329: 571-575, 2010.
15. Gourine AV, Llaudet E, Dale N, Spyer KM. ATP is a mediator of chemosensory transduction in the central nervous system. Nature 436: 108-111, 2005.
16. Grass D, Pawlowski PG, Hirrlinger J, Papadopoulos N, Richter DW, Kirchhoff F, Hulsmann S. Diversity of functional astroglial properties in the respiratory network. J Neurosci 24: 1358-1365, 2004.
17. -:1 Na(+). J Physiol 531: 375-382, 2001.
18. + channel subunits, Kir4.1 and Kir5.1, in brain astrocytes. J Biol Chem 279: 44065-44073, 2004.
19. Holleran J, Babbie M, Erlichman JS. Ventilatory effects of impaired glial function in a brain stem chemoreceptor region in the conscious rat. J Appl Physiol 90: 1539-1547, 2001.
20. Jiang C, Xu H, Cui N, Wu J. An alternative approach to the identification of respiratory central chemoreceptors in the brainstem. Respir Physiol 129: 141-157, 2001.
21. Kubo Y, Adelman JP, Clapham DE, Jan LY, Karschin A, Kurachi Y, Lazdunski M, Nichols CG, Seino S, Vandenberg CA. International Union of Pharmacology. LIV. Nomenclature and molecular relationship of inwardly rectifying potassium channels. Pharmacol Rev 57: 509-526, 2005. (Pubitemid 43036438)
22. Matthias K, Kirchhoff F, Seifert G, Huttmann K, Matyash M, Kettenmann H, Steinhauser C. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 23: 1750-1758, 2003.
23. Millhorn DE, Eldridge FL, Kiley JP. Oscillations of medullary extracellular fluid pH caused by breathing. Respir Physiol 55: 193-203, 1984.
24. Mulkey DK, Mistry AM, Guyenet PG, Bayliss DA. Purinergic P2 receptors modulate excitability but do not mediate pH sensitivity of RTN respiratory chemoreceptors. J Neurosci 26: 7230-7233, 2006.
25. Mulkey DK, Stornetta RL, Weston MC, Simmons JR, Parker A, Bayliss DA, Guyenet PG. Respiratory control by ventral surface chemoreceptor neurons in rats. Nat Neurosci 7: 1360-1369, 2004.
26. Mulkey DK, Talley EM, Stornetta RL, Siegel AR, West GH, Chen X, Sen N, Mistry AM, Guyenet PG, Bayliss DA. TASK channels determine pH sensitivity in select respiratory neurons but do not contribute to central respiratory chemosensitivity. J Neurosci 27: 14049-14058, 2007.
27. Munsch T, Deitmer JW. Sodium-bicarbonate cotransport current in identified leech glial cells. J Physiol 474: 43-53, 1994.
28. Newman EA. Sodium-bicarbonate cotransport in retinal Muller (glial) cells of the salamander. J Neurosci 11: 3972-3983, 1991.
29. + buffering to cell differentiation. J Neurochem 107: 589-601, 2008.
30. + channels. Trends Neurosci 24: 339-346, 2001.
31. Pessia M, Imbrici P, D'Adamo MC, Salvatore L, Tucker SJ. Differential pH sensitivity of Kir4.1 and Kir4.2 potassium channels and their modulation by heteropolymerisation with Kir5.1. J Physiol 532: 359-367, 2001.
32. + channels. EMBO J 15: 2980-2987, 1996.
33. 2 and acid signaling in chemosensitive neurons. Am J Physiol Cell Physiol 287: C1493-C1526, 2004.
34. Ritucci NA, Erlichman JS, Leiter JC, Putnam RW. Response of membrane potential and intracellular pH to hypercapnia in neurons and astrocytes from rat retrotrapezoid nucleus. Am J Physiol Regul Integr Comp Physiol 289: R851-R861, 2005.
35. Schultz JH, Czachurski J, Volk T, Ehmke H, Seller H. Central sympathetic chemosensitivity and Kir1 potassium channels in the cat. Brain Res 963: 113-120, 2003.
36. Spyer KM. To breathe or not to breathe? That is the question. Exp Physiol 94: 1-10, 2009.
37. Su S, Ohno Y, Lossin C, Hibino H, Inanobe A, Kurachi Y. Inhibition of astroglial inwardly rectifying Kir4.1 channels by a tricyclic antidepressant, nortriptyline. J Pharmacol Exp Ther 320: 573-580, 2007.
38. Tang X, Taniguchi K, Kofuji P. Heterogeneity of Kir4.1 channel expression in glia revealed by mouse transgenesis. Glia 57: 1706-1715, 2009.
39. + channels to central chemosensitivity in cultivated neurons of fetal rat medulla. J Neurophysiol 79: 2885-2894, 1998.
40. 2-sensitive Kir channels in brainstem neurons of rats. J Membr Biol 197: 179-191, 2004.
41. Xu H, Cui N, Yang Z, Qu Z, Jiang C. Modulation of Kir4.1 and Kir5.1 by hypercapnia and intracellular acidosis. J Physiol 524: 725-735, 2000.
42. Xu H, Yang Z, Cui N, Giwa LR, Abdulkadir L, Patel M, Sharma P, Shan G, Shen W, Jiang C. Molecular determinants for the distinct pH sensitivity of Kir1.1 and Kir4.1 channels. Am J Physiol Cell Physiol 279: C1464-C1471, 2000.
43. 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.
44. Zhou M, Xu G, Xie M, Zhang X, Schools 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.
45. 2 inhibits specific inward rectifier K(+) channels by decreases in intra- and extracellular pH. J Cell Physiol 183: 53-64, 2000.