Downregulation of the potassium chloride cotransporter KCC2 in vulnerable motoneurons in the SOD1-G93A mouse model of amyotrophic lateral sclerosis

Journal of Neuropathology and Experimental Neurology

Volumn 69, Issue 10, 2010, Pages 1057-1070

  Fuchs, Andrea ^a   Ringer, Cornelia ^b   Bilkei Gorzo, Andras ^c   Weihe, Eberhard ^b   Roeper, Jochen ^a   Schütz, Burkhard ^b  

^a GOETHE UNIVERSITY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c Life and Brain Center   (Germany)

Author keywords

Amyotrophic lateral sclerosis; Hypoglossal nucleus; KCC2; Motoneuron; Neurodegeneration; NKCC1

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; COPPER ZINC SUPEROXIDE DISMUTASE; GLYCINE RECEPTOR; POTASSIUM CHLORIDE COTRANSPORTER; POTASSIUM CHLORIDE COTRANSPORTER 2; SODIUM POTASSIUM CHLORIDE COTRANSPORTER; UNCLASSIFIED DRUG; COTRANSPORTER; MESSENGER RNA; POTASSIUM-CHLORIDE SYMPORTERS; SLC18A3 PROTEIN, MOUSE; SOD1 G93A PROTEIN; SUPEROXIDE DISMUTASE; VESICULAR ACETYLCHOLINE TRANSPORTER;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; DISEASE COURSE; DOWN REGULATION; EXCITOTOXICITY; FEMALE; IMMUNOREACTIVITY; LUMBAR SPINAL CORD; MALE; MOTONEURON; MOUSE; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPTIC INHIBITION; AGE; ANALYSIS OF VARIANCE; ANIMAL; BRAIN STEM; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; SPINAL CORD; TRANSGENIC MOUSE;

AGE FACTORS; AMYOTROPHIC LATERAL SCLEROSIS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BRAIN STEM; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MALE; MICE; MICE, TRANSGENIC; MOTOR NEURONS; RNA, MESSENGER; SPINAL CORD; SUPEROXIDE DISMUTASE; SYMPORTERS; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

EID: 77957933412     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3181f4dcef     Document Type: Article

References (43)

1. Rowland LP, Shneider NA. Amyotrophic lateral sclerosis. N Engl J Med 2001;344:1688-700
2. Rothstein JD. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann Neurol 2009;65(suppl 1):S3-9
3. Van Damme P, Dewil M, Robberecht W, et al. Excitotoxicity and amyotrophic lateral sclerosis. Neurodegener Dis 2005;2:147-59
4. Pieri M, Albo F, Gaetti C, et al. Altered excitability of motor neurons in a transgenic mouse model of familial amyotrophic lateral sclerosis. Neurosci Lett 2003;351:153-56
5. Kanai K, Kuwabara S, Misawa S, et al. Altered axonal excitability properties in amyotrophic lateral sclerosis: Impaired potassium channel function related to disease stage. Brain 2006;129:953-62
6. Kaduri AJ, Magoul R, Lescaudron L, et al. Immunocytochemical approach of GABAergic innervation of the mouse spinal cord using antibodies to GABA. J Hirnforsch 1987;28:349-55
7. Hebert SC, Mount DB, Gamba G. Molecular physiology of cationcoupled Clj cotransport: The SLC12 family. Pflugers Arch 2004;447: 580-93
8. Blaesse P, Airaksinen MS, Rivera C, et al. Cation-chloride cotransporters and neuronal function. Neuron 2009;61:820-38
9. Li H, Tornberg J, Kaila K, et al. Patterns of cation-chloride cotransporter expression during embryonic rodent CNS development. Eur J Neurosci 2002;16:2358-70
10. Payne JA, Stevenson TJ, Donaldson LF. Molecular characterization of a putative K-Cl cotransporter in rat brain. A neuronal-specific isoform. J Biol Chem 1996;271:16245-52
11. Rivera C, Voipio J, Payne JA, et al. The K+/Clj co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999;397:251-55
12. Kanaka C, Ohno K, Okabe A, et al. The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC1,2) and NaYK-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience 2001;104:933-46
13. Achilles K, Okabe A, Ikeda M, et al. Kinetic properties of Cl uptake mediated by Na+-dependent K+-2Cl cotransport in immature rat neocortical neurons. J Neurosci 2007;27:8616-27
14. Stein V, Hermans-Borgmeyer I, Jentsch TJ, et al. Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 2004;468:57-64
15. Delpy A, Allain AE, Meyrand P, et al. NKCC1 cotransporter inactivation underlies embryonic development of chloride-mediated inhibition in mouse spinal motoneuron. J Physiol 2008;586:1059-75
16. Kahle KT, Staley KJ, Nahed BV, et al. Roles of the cation-chloride cotransporters in neurological disease. Nat Clin Pract Neurol 2008;4: 490-503
17. Boulenguez P, Liabeuf S, Bos R, et al. Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nat Med 2010;16:302-7
18. Gurney ME, Pu H, Chiu AY, et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994;264:1772-75
19. Schutz B, Reimann J, Dumitrescu-Ozimek L, et al. The oral antidiabetic pioglitazone protects from neurodegeneration and amyotrophic lateral sclerosisYlike symptoms in superoxide dismutaseYG93A transgenic mice. J Neurosci 2005;25:7805-12
20. Hayar A, Bryant JL, Boughter JD, et al. A low-cost solution to measure mouse licking in an electrophysiological setup with a standard analogto- digital converter. J Neurosci Methods 2006;153:203-7
21. Schutz B, von Engelhardt J, Gordes M, et al. Sweat gland innervation is pioneered by sympathetic neurons expressing a cholinergic/noradrenergic co-phenotype in the mouse. Neuroscience 2008;156:310-18
22. Hubner CA, Stein V, Hermans-Borgmeyer I, et al. Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 2001;30:515-24
23. Schutz B, Chen L, Schafer MK, et al. Somatomotor neuronYspecific expression of the human cholinergic gene locus in transgenic mice. Neuroscience 2000;96:707-22
24. Schafer MK, Varoqui H, Defamie N, et al. Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J Biol Chem 2002;277: 50734-48
25. Stil A, Liabeuf S, Jean-Xavier C, et al. Developmental up-regulation of the potassium-chloride cotransporter type 2 in the rat lumbar spinal cord. Neuroscience 2009;164:809-21
26. Palma E, Amici M, Sobrero F, et al. Anomalous levels of Clj transporters in the hippocampal subiculum from temporal lobe epilepsy patients make GABA excitatory. Proc Natl Acad Sci U S A 2006;103: 8465-68
27. Toyoda H, Ohno K, Yamada J, et al. Induction of NMDA and GABAA receptorYmediated Ca2+ oscillations with KCC2 mRNA downregulation in injured facial motoneurons. J Neurophysiol 2003;89:1353-62
28. Haenggeli C, Kato AC. Differential vulnerability of cranial motoneurons in mouse models with motor neuron degeneration. Neurosci Lett 2002; 335:39-43
29. Angenstein F, Niessen HG, Goldschmidt J, et al. Age-dependent changes in MRI of motor brain stem nuclei in a mouse model of ALS. Neuroreport 2004;15:2271-74
30. Erickson JD, Varoqui H, Schafer MK, et al. Functional identification of a vesicular acetylcholine transporter and its expression from a Bcholinergic[ gene locus. J Biol Chem 1994;269:21929-32
31. Van Damme P, Callewaert G, Eggermont J, et al. Chloride influx aggravates Ca2+-dependent AMPA receptorYmediated motoneuron death. J Neurosci 2003;23:4942-50
32. Prescott SA, Sejnowski TJ, De Koninck Y. Reduction of anion reversal potential subverts the inhibitory control of firing rate in spinal lamina I neurons: Towards a biophysical basis for neuropathic pain. Mol Pain 2006;2:32
33. De Koninck Y. Altered chloride homeostasis in neurological disorders: A new target. Curr Opin Pharmacol 2007;7:93-99
34. Schutz B. Imbalanced excitatory to inhibitory synaptic input precedes motor neuron degeneration in an animal model of amyotrophic lateral sclerosis. Neurobiol Dis 2005;20:131-40
35. Kelsch W, Hormuzdi S, Straube E, et al. Insulin-like growth factor 1 and a cytosolic tyrosine kinase activate chloride outward transport during maturation of hippocampal neurons. J Neurosci 2001;21:8339-47
36. Lee HH, Walker JA, Williams JR, et al. Direct protein kinase CYdependent phosphorylation regulates the cell surface stability and activity of the potassium chloride cotransporter KCC2. J Biol Chem 2007;282:29777-84
37. Kiernan JA, Hudson AJ. Changes in sizes of cortical and lower motor neurons in amyotrophic lateral sclerosis. Brain 1991;114:843-53
38. Wake H, Watanabe M, Moorhouse AJ, et al. Early changes in KCC2 phosphorylation in response to neuronal stress result in functional downregulation. J Neurosci 2007;27:1642-50
39. Lobsiger CS, Cleveland DW. Glial cells as intrinsic components of nonY cell-autonomous neurodegenerative disease. Nat Neurosci 2007;10:1355-60
40. Henkel JS, Beers DR, Zhao W, et al. Microglia in ALS: The good, the bad, and the resting. J Neuroimmune Pharmacol 2009;4:389-98
41. Rivera C, Li H, Thomas-Crusells J, et al. BDNF-induced TrkB activation down-regulates the K+-Clj cotransporter KCC2 and impairs neuronal Clj extrusion. J Cell Biol 2002;159:747-52
42. Coull JA, Beggs S, Boudreau D, et al. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 2005;438:1017-21
43. Ben-Ari Y. Excitatory actions of GABA during development: The nature of the nurture. Nat Rev Neurosci 2002;3:728-39