Malfunction of respiratory-related neuronal activity in Na+, K+-ATPase α2 subunit-deficient mice is attributable to abnormal Cl- homeostasis in brainstem neurons

Journal of Neuroscience

Volumn 24, Issue 47, 2004, Pages 10693-10701

  Ikeda, Keiko ^a   Onimaru, Hiroshi ^b   Yamada, Junko ^c   Inoue, Koichi ^d   Ueno, Shinya ^d   Onaka, Tatsushi ^a   Toyoda, Hiroki ^a   Arata, Akiko ^e   Ishikawa, Tomo O ^f,g   Taketo, Makoto M ^f,g   Fukuda, Atsuo ^c,d   Kawakami, Kiyoshi ^a  

^a JICHI MEDICAL UNIVERSITY   (Japan)

^b SHOWA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c SHIZUOKA UNIVERSITY   (Japan)

^d HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^f KYOTO UNIVERSITY   (Japan)

^g TAIHO PHARMACEUTICAL CO LTD   (Japan)

Author keywords

Cl i; Brainstem spinal cord preparation; GABA; KCC2; Na, K ATPase; Respiratory neuron

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CHLORIDE; GRAMICIDIN;

ANIMAL CELL; ARTICLE; ATP1ALPHA2 GENE; BRAIN STEM; BREATHING; BREATHING DISORDER; CONTROLLED STUDY; CYTOSOL; ELECTROSTIMULATION; ENZYME DEFICIENCY; HOMEOSTASIS; KNOCKOUT GENE; KNOCKOUT MOUSE; MEDULLA OBLONGATA; MOTONEURON; MOUSE; NERVE CELL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RESPIRATION CENTER;

AMINO ACID SEQUENCE; ANIMALS; APNEA; CHLORIDES; ELECTRIC STIMULATION; FACIAL NERVE; FETUS; GAMMA-AMINOBUTYRIC ACID; HOMEOSTASIS; ISOENZYMES; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; NA(+)-K(+)-EXCHANGING ATPASE; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM; RESPIRATORY CENTER; SPINAL NERVE ROOTS; SYMPORTERS;

EID: 9344231411     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2909-04.2004     Document Type: Article

References (50)

1. Abe Y, Furukawa K, Itoyama Y, Akaike N (1994) Glycine response in acutely dissociated ventromedial hypothalamic neuron of the rat: new approach with gramicidin perforated patch-clamp technique. J Neurophysiol 72:1530-1537.
2. Ballanyi K, Onimaru H, Homma I (1999) Respiratory network function in the isolated brainstem-spinal cord of newborn rats. Prog Neurobiol 59:583-634.
3. A receptors: classification on the basis of subunit structure and receptor function. Pharmacol Rev 50:291-313.
4. Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.
5. Blanco G, Koster JC, Sánchez G, Mercer RW (1995) Kinetic properties of the α2β1 and α2β2 isozymes of the Na,K-ATPase. Biochemistry 34:319-325.
6. Brockhaus J, Ballanyi K (1998) Synaptic inhibition in the isolated respiratory network of neonatal rats. Eur J Neurosci 10:3823-3839.
7. +-ATPase) distribution in the synaptic regions in the cerebral cortex of rats. Neurosci Res 24:309-312.
8. Feldman JL, Mitchell GS, Nattie EE (2003) Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci 26:239-266.
9. 2+ signaling. Am J Physiol 284:C475-C486.
10. Gorini A, Canosi U, Devecchi E, Geroldi D, Villa RF (2002) ATPases enzyme activities during ageing in different types of somatic and synaptic plasma membranes from rat frontal cerebral cortex. Prog Neuropsychopharmacol Biol Psychiatry 26:81-90.
11. Gray PA, Janczewski WA, Mellen N, McCrimmon DR, Feldman JL (2001) Normal breathing requires preBötzinger complex neurokinin-1 receptor-expressing neurons. Nat Neurosci 4:927-930.
12. A receptor-mediated inhibition in rat substantia nigra. J Neurosci 23:8237-8246.
13. Gulyás AI, Sík A, Payne JA, Kaila K, Freund TF (2001) The KCl cotransporter, KCC2, is highly expressed in the vicinity of excitatory synapses in the rat hippocampus. Eur J Neurosci 13:2205-2217.
14. Hartford AK, Messer ML, Moseley AE, Lingrel JB, Delamere NA (2004) Na,K-ATPase α2 inhibition alters calcium responses in optic nerve astrocytes. Glia 45:229-237.
15. 3-isoform gene expression. Am J Physiol 266:C1301-C1312.
16. Hübner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, Jentsch TJ (2001) Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30:515-524.
17. Ikeda K, Onaka T, Yamakado M, Nakai J, Ishikawa T, Taketo MM, Kawakami K (2003) Degeneration of the amygdala/piriform cortex and enhanced fear/anxiety behaviors in sodium pump α2 subunit (Atp1a2)-deficient mice. J Neurosci 23:4667-4676.
18. 3 isoforms expressed in HeLa cells. J Biol Chem 266:16925-16930.
19. A receptor channel function in the nervous system. Prog Neurobiol 42:489-537.
20. Lencesova L, O'Neill A, Resneck WG, Bloch RJ, Blaustein MP (2004) Plasma membrane-cytoskeleton-endoplasmic reticulum complexes in neurons and astrocytes. J Biol Chem 279:2885-2893.
21. Li H, Tornberg J, Kaila K, Airaksinen MS, Rivera C (2002) Patterns of cation-chloride cotransporter expression during embryonic rodent CNS development. Eur J Neurosci 16:2358-2370.
22. Lingrel J, Moseley A, Dostanic I, Cougnon M, He S, James P, Woo A, O'Connor K, Neumann J (2003) Functional roles of the α isoforms of the Na,K-ATPase. Ann NY Acad Sci 986:354-359.
23. LoTurco JJ, Owens DF, Heath MJS, Davis MBE, Kriegstein AR (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287-1298.
24. Moseley AE, Lieske SP, Wetzel RK, James PF, He S, Shelly DA, Paul RJ, Boivin GP, Witte DP, Ramirez JM, Sweadner KJ, Lingrel JB (2003) The Na,K-ATPase α2 isoform is expressed in neurons, and its absence disrupts neuronal activity in newborn mice. J Biol Chem 278:5317-5324.
25. A receptor-mediated excitation after in vivo axonal injury. J Neurosci 22:4412-4417.
26. Onimaru H, Homma I (2003) A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 23:1478-1486.
27. Otis TS, Staley KJ, Mody I (1991) Perpetual inhibitory activity in mammalian brain slices generated by spontaneous GABA release. Brain Res 545:142-150.
28. Owens DF, Kriegstein AR (2002) Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3:715-727.
29. o regulation. Am J Physiol 273:C1516-C1525.
30. Payne JA, Stevenson TJ, Donaldson LF (1996) Molecular characterization of a putative K-Cl cotransporter in rat brain. A neuronal-specific isoform. J Biol Chem 271:16245-16252.
31. Payne JA, Rivera C, Voipio J, Kaila K (2003) Cation-chloride co-tansporters in neuronal communication, development and trauma. Trends Neurosci 26:199-206.
32. Peng L, Martin-Vasallo P, Sweadner KJ (1997) Isoforms of Na,K-ATPase α and β subunits in the rat cerebellum and in granule cell cultures. J Neurosci 17:3488-3502.
33. Richter DW, Spyer KM (2001) Studying rhythmogenesis of breathing: comparison of in vivo and in vitro models. Trends Neurosci 24:464-472.
34. A-mediated inhibition in the brainstem respiratory rhythm-generating network of the mouse. Eur J Neurosci 12:2975-2984.
35. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251-255.
36. 2-isoform specifically couples to contractility in vascular smooth muscle: evidence from gene-targeted neonatal mice. Am J Physiol 286:C813-C820.
37. +-ATPase α-subunit from rat brain. Biochemistry 25:8125-8132.
38. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL (1991) Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254:726-729.
39. Stein V, Hermans-Borgmeyer I, Jentsch TJ, Hübner CA (2004) Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 468:57-64.
40. Stell B, Mody I (2003) A tale of timing and transport. Neuron 39:729-730.
41. +-ATPase. Biochim Biophys Acta 988:185-220.
42. Sweadner KJ (1992) Overlapping and diverse distribution of Na-K ATPase isozymes in neurons and glia. Can J Physiol Pharmacol 70:5255-5259.
43. 2+ oscillations with KCC2 mRNA downregulation in injured facial motoneurons. J Neurophysiol 89:1353-1362.
44. Verbeugen JAH, Fricker D, Miles R (1999) Noninvasive measurements of the membrane potential and GABAergic action in hippocampal interneurons. J Neurosci 19:2546-2555.
45. Vu TQ, Payne JA, Copenhagen DR (2000) Localization and developmental expression patterns of the neuronal K-Cl cotransporter (KCC2) in the rat retina. J Neurosci 20:1414-1423.
46. Wang C, Shimizu-Okabe C, Watanabe K, Okabe A, Matsuzaki H, Ogawa T, Mori N, Fukuda A, Sato K (2002) Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Dev Brain Res 139:59-66.
47. Williams JR, Sharp JW, Kumari VG, Wilson M, Payne JA (1999) The neuron-specific K-Cl cotransporter, KCC2. Antibody development and initial characterization of the protein. J Biol Chem 274:12656-12664.
48. Woo N-S, Lu J, England R, McClellan R, Dufour S, Mount DB, Deutch AY, Lovinger DM, Delpire E (2002) Hyperexcitability and epilepsy associated with disruption of the mouse neuronal-specific K-Cl cotransporter gene. Hippocampus 12:258-268.
49. - transporter activity. Neuron 39:807-820.
50. - uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol (Lond) 557:829-841.