Differential effects on KCC2 expression and spasticity of ALS and traumatic injuries to motoneurons

Frontiers in Cellular Neuroscience

Volumn 8, Issue JAN, 2014, Pages

  Mòdol, Laura ^a   Mancuso, Renzo ^a   Alé, Albert ^a   Francos Quijorna, Isaac ^a   Navarro, Xavier ^a  

^a INSTITUT DE NEUROCIÈNCIES   (Spain)

Author keywords

Hypereflexia; KCC2 transporter; Motoneuron disease; SOD1G93A mice; Spasticity

Indexed keywords

CALBINDIN; GEPHYRIN; POTASSIUM CHLORIDE COTRANSPORTER; POTASSIUM CHLORIDE COTRANSPORTER 2; SEROTONIN; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; EVOKED MUSCLE RESPONSE; FEMALE; FUNCTIONAL ASSESSMENT; HYPERREFLEXIA; IMMUNOHISTOCHEMISTRY; LOCOMOTION; LUMBAR SPINAL CORD; MICROGLIA; MOTONEURON; MOTOR NERVE CONDUCTION; MOUSE; NERVE CELL DEGENERATION; NERVE CELL LESION; NERVE FIBER; NONHUMAN; PROTEIN EXPRESSION; RENSHAW CELL; SCIATIC NERVE INJURY; SPASTICITY; SPINAL CORD INJURY; WESTERN BLOTTING;

EID: 84892950294     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00007     Document Type: Article

References (61)

1. Alvarez, F. J., and Fyffe, R. E. W. (2007). The continuing case for the Renshaw cell. J. Physiol. 584, 31-45. doi: 10.1113/jphysiol.2007.136200
2. Basso, D. M., Fisher, L. C., Anderson, A. J., Jakeman, L. B., McTigue, D. M., and Popovich, P. G. (2006). Basso mouse scale for locomotion detects differences in recovery after spinal cord injury in five five common mouse strains. J. Neurotrauma 23, 635-659. doi: 10.1089/neu.2006.23.635
3. Ben-Ari, Y., Gaiarsa, J.-L., Tyzio, R., and Khazipov, R. (2007). GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87, 1215-1284. doi: 10.1152/physrev.00017.2006
4. Blaesse, P., Guillemin, I., Schindler, J., Schweizer, M., Delpire, E., Khiroug, L., et al. (2006). Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. J. Neurosci. 26, 10407-10419. doi: 10.1523/JNEUROSCI.3257-06.2006
5. Boërio, D., Kalmar, B., Greensmith, L., and Bostock, H. (2010). Excitability properties of mouse motor axons in the mutant SOD1(G93A) model of amyotrophic lateral sclerosis. Muscle Nerve. 41, 774-784. doi: 10.1002/mus.21579
6. Bohlhalter, S., Möhler, H., and Fritschy, J. M. (1994). Inhibitory neurotransmission in rat spinal cord: co-localization of glycine-and GABAA-receptors at GABAergic synaptic contacts demonstrated by triple immunofluorescence staining. Brain Res. 642, 59-69. doi: 10.1016/0006-8993(94)90905-9
7. Bos, R., Sadlaoud, K., Boulenguez, P., Buttigieg, D., Liabeuf, S., Brocard, C., et al. (2013). Activation of 5-HT2A receptors upregulates the function of the neuronal K-Cl cotransporter KCC2. Proc. Natl. Acad. Sci. U.S.A. 110, 348-353. doi: 10.1073/pnas.1213680110
8. Bosco, D. A., Morfini, G., Karabacak, N. M., Song, Y., Gros-Louis, F., Pasinelli, P., et al. (2010). Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat. Neurosci. 13, 1396-1403. doi: 10.1038/nn.2660
9. Boulenguez, P., Liabeuf, S., Bos, R., Bras, H., Jean-Xavier, C., Brocard, C., et al. (2010). Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nat. Med. 16, 302-307. doi: 10.1038/nm.2107
10. Bray, J. G., and Mynlieff, M. (2009). Influx of calcium through L-type calcium channels in early postnatal regulation of chloride transporters in the rat hippocampus. Dev. Neurobiol. 69, 885-896. doi: 10.1002/dneu.20749
11. Chang, Q., and Martin, L. J. (2009). Glycinergic innervation of motoneurons is deficient in amyotrophic lateral sclerosis mice: a quantitative confocal analysis. Am. J. Pathol. 174, 574-585. doi: 10.2353/ajpath.2009.080557
12. Chang, Q., and Martin, L. J. (2011). Glycine receptor channels in spinal motoneurons are abnormal in a transgenic mouse model of amyotrophic lateral sclerosis. J. Neurosci. 31, 2815-2827. doi: 10.1523/JNEUROSCI.2475-10.2011
13. Coull, J. A. M., Beggs, S., Boudreau, D., Boivin, D., Tsuda, M., Inoue, K., et al. (2005). BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438, 1017-1021. doi: 10.1038/nature04223
14. Coull, J. A. M., Boudreau, D., Bachand, K., Prescott, S. A., Nault, F., Sik, A., et al. (2003). Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 424, 938-942. doi: 10.1038/nature01868
15. Cramer, S. W., Baggott, C., Cain, J., Tilghman, J., Allcock, B., Miranpuri, G., et al. (2008). The role of cation-dependent chloride transporters in neuropathic pain following spinal cord injury. Mol. Pain. 4, 36. doi: 10.1186/1744-8069-4-36
16. Dentel, C., Palamiuc, L., Henriques, A., Lannes, B., Spreux-Varoquaux, O., Gutknecht, L., et al. (2013). Degeneration of serotonergic neurons in amyotrophic lateral sclerosis: a link to spasticity. Brain 136, 483-493. doi: 10.1093/brain/aws274
17. Ferrini, F., and De Koninck, Y. (2013). Microglia control neuronal network excitability via BDNF signalling. Neural Plast. 2013, 429815. doi: 10.1155/2013/429815
18. - homeostasis. Nat. Neurosci. 16, 183-192. doi: 10.1038/nn.3295
19. Fu, S. Y., and Gordon, T. (1997). The cellular and molecular basis of peripheral nerve regeneration. Mol. Neurobiol. 14, 67-116. doi: 10.1007/BF02740621
20. Fuchs, A., Ringer, C., Bilkei-Gorzo, A., Weihe, E., Roeper, J., and Schütz, B. (2010). Downregulation of the potassium chloride cotransporter KCC2 in vulnerable motoneurons in the SOD1-G93A mouse model of amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 69, 1057-1070. doi: 10.1097/NEN.0b013e3181f4dcef
21. Ganguly, K., Schinder, A. F., Wong, S. T., and Poo, M. (2001). GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105, 521-532. doi: 10.1016/S0092-8674(01)00341-5
22. García-Alías, G., Verdú, E., Forés, J., López-Vales, R., and Navarro, X. (2003). Functional and electrophysiological characterization of photochemical graded spinal cord injury in the rat. J. Neurotrauma 20, 501-510. doi: 10.1089/089771503765355568
23. Hasbargen, T., Ahmed, M. M., Miranpuri, G., Li, L., Kahle, K. T., Resnick, D., et al. (2010). Role of NKCC1 and KCC2 in the development of chronic neuropathic pain following spinal cord injury. Ann. N. Y Acad. Sci. 1198, 168-172. doi: 10.1111/j.1749-6632.2010.05462.x
24. Heckman, C. J., Lee, R. H., and Brownstone, R. M. (2003). Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior. Trends Neurosci. 26, 688-895. doi: 10.1016/j.tins.2003.10.002
25. Janssen, S. P., Gerard, S., Raijmakers, M. E., Truin, M., Van Kleef, M., and Joosten, E. A. (2012). Decreased intracellular GABA levels contribute to spinal cord stimulation-induced analgesia in rats suffering from painful peripheral neuropathy: the role of KCC2 and GABA(A) receptor-mediated inhibition. Neurochem. Int. 60, 21-30. doi: 10.1016/j.neuint.2011.11.006
26. Janssen, S. P., Truin, M., Van Kleef, M., and Joosten, E. A. (2011). Differential GABAergic disinhibition during the development of painful peripheral neuropathy. Neuroscience 184, 183-194. doi: 10.1016/j.neuroscience.2011.03.060
27. Julien, J. P. (1997). Neurofilaments and motor neuron disease. Trends Cell Biol. 7, 243-249. doi: 10.1016/S0962-8924(97)01049-0
28. Kakinohana, O., Scadeng, M., Corleto, J. A., Sevc, J., Lukacova, N., and Marsala, M. (2012). Development of AMPA receptor and GABA B receptor-sensitive spinal hyper-reflexia after spinal air embolism in rat: a systematic neurological, electrophysiological and qualitative histopathological study. Exp. Neurol. 237, 26-35. doi: 10.1016/j.expneurol.2012.06.004
29. Katz, R., and Pierrot-Deseilligny, E. (1999). Recurrent inhibition in humans. Prog. Neurobiol. 57, 325-355. doi: 10.1016/S0301-0082(98)00056-2
30. Kiernan, M. C., Vucic, S., Cheah, B. C., Turner, M. R., Eisen, A., Hardiman, O., et al. (2011). Amyotrophic lateral sclerosis. Lancet 377, 942-955. doi: 10.1016/S0140-6736(10)61156-7
31. Klopstein, A., Santos-Nogueira, E., Francos-Quijorna, I., Redensek, A., David, S., Navarro, X., et al. (2012). Beneficial effects of B-crystallin in spinal cord contusion injury. J. Neurosci. 32, 14478-14488. doi: 10.1523/JNEUROSCI.0923-12.2012
32. Lance, J. W. (1980). The control of muscle tone, reflexes, and movement: Robert Wartenberg lecture. Neurology 30, 1303-1313. doi: 10.1212/WNL.30.12.1303
33. Lee, H. H. C., Jurd, R., and Moss, S. J. (2010). Tyrosine phosphorylation regulates the membrane trafficking of the potassium chloride co-transporter KCC2. Mol. Cell. Neurosci. 45, 173-179. doi: 10.1016/j.mcn.2010.06.008
34. Lee, H. H. C., Walker, J. A., Williams, J. R., Goodier, R. J., Payne, J. A., and Moss, S. J. (2007). Direct protein kinase C-dependent phosphorylation regulates the cell surface stability and activity of the potassium chloride cotransporter KCC2. J. Biol. Chem. 282, 29777-29784. doi: 10.1074/jbc.M705053200
35. Lévi, S., Logan, S. M., Tovar, K. R., and Craig, A. M. (2004). Gephyrin is critical for glycine receptor clustering but not for the formation of functional GABAergic synapses in hippocampal neurons. J. Neurosci. 24, 207-217. doi: 10.1523/JNEUROSCI.1661-03.2004
36. Li, H., Khirug, S., Cai, C., Ludwig, A., Blaesse, P., Kolikova, J., et al. (2007). KCC2 interacts with the dendritic cytoskeleton to promote spine development. Neuron 56, 1019-1033. doi: 10.1016/j.neuron.2007.10.039
37. Lu, Y., Zheng, J., Xiong, L., Zimmermann, M., and Yang, J. (2008). Spinal cord injury-induced attenuation of GABAergic inhibition in spinal dorsal horn circuits is associated with down-regulation of the chloride transporter KCC2 in rat. J. Physiol. 586, 5701-5715. doi: 10.1113/jphysiol.2008.152348
38. Mancuso, R., Oliván, S., Rando, A., Casas, C., Osta, R., and Navarro, X. (2012). Sigma-1R agonist improves motor function and motoneuron survival in ALS mice. Neurotherapeutics 9, 814-826. doi: 10.1007/s13311-012-0140-y
39. Mancuso, R., Santos-Nogueira, E., Osta, R., and Navarro, X. (2011). Electrophysiological analysis of a murine model of motoneuron disease. Clin. Neurophysiol. 122, 1660-1670. doi: 10.1016/j.clinph.2011.01.045
40. Mazzocchio, R., and Rossi, A. (1997). Involvement of spinal recurrent inhibition in spasticity. Further insight into the regulation of Renshaw cell activity. Brain. 120, 991-1003. doi: 10.1093/brain/120.6.991
41. Mazzocchio, R., and Rossi, A. (2010). Role of Renshaw cells in amyotrophic lateral sclerosis. Muscle Nerve. 41, 441-443. doi: 10.1002/mus.21602
42. Murray, K. C., Nakae, A., Stephens, M. J., Rank, M., D'Amico, J., Harvey, P. J., et al. (2010). Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT. Nat. Med. 16, 694-700. doi: 10.1038/nm.2160
43. Murray, K. C., Stephens, M. J., Ballou, E. W., Heckman, C. J., and Bennett, D. J. (2011). Motoneuron excitability and muscle spasms are regulated by 5-HT2B and 5-HT2C receptor activity. J. Neurophysiol. 105, 731-748. doi: 10.1152/jn.00774.2010
44. Navarro, X., Vivó, M., and Valero-Cabré, A. (2007). Neural plasticity after peripheral nerve injury and regeneration. Prog. Neurobiol. 82, 163-201. doi: 10.1016/j.pneurobio.2007.06.005
45. Payne, J. A., Rivera, C., Voipio, J., and Kaila, K. (2003). Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci. 26, 199-206. doi: 10.1016/S0166-2236(03)00068-7
46. Pieraut, S., Laurent-Matha, V., Sar, C., Hubert, T., Méchaly, I., Hilaire, C., et al. (2007). NKCC1 phosphorylation stimulates neurite growth of injured adult sensory neurons. J. Neurosci. 27, 6751-6759. doi: 10.1523/JNEUROSCI.1337-07.2007
47. Pieraut, S., Lucas, O., Sangari, S., Sar, C., Boudes, M., Bouffi, C., et al. (2011). An autocrine neuronal Interleukin-6 loop mediates chloride accumulation and NKCC1 phosphorylation in axotomized sensory neurons. J. Neurosci. 31, 13516-13526. doi: 10.1523/JNEUROSCI.3382-11.2011
48. Ripps, M. E., Huntley, G. W., Hof, P. R., Morrison, J. H., and Gordon, J. W. (1995). Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U.S.A. 92, 689-693. doi: 10.1073/pnas.92.3.689
49. Rivera, C., Li, H., Thomas-Crusells, J., Lahtinen, H., Viitanen, T., Nanobashvili, A., et al. (2002). BDNF-induced TrkB activation down-regulates the K+-Cl-cotransporter KCC2 and impairs neuronal Cl-extrusion. J. Cell Biol. 159, 747-752. doi: 10.1083/jcb.200209011
50. Rivera, C., Voipio, J., Payne, J. A., Ruusuvuori, E., Lahtinen, H., Lamsa, K., et al. (1999). The K+/Cl-co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397, 251-255. doi: 10.1038/16697
51. Rosen, D. R. (1993). Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 364, 362. doi: 10.1038/362059a0
52. Saxena, S., Cabuy, E., and Caroni, P. (2009). A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat. Neurosci. 12, 627-636. doi: 10.1038/nn.2297
53. Schütz, B. (2005). Imbalanced excitatory to inhibitory synaptic input precedes motor neuron degeneration in an animal model of amyotrophic lateral sclerosis. Neurobiol. Dis. 20, 131-140. doi: 10.1016/j.nbd.2005.02.006
54. Stein, V., Hermans Borgmeyer, I., Jentsch, T. J., and Hübner, C. A. (2004). Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J. Comp. Neurol. 468, 57-64. doi: 10.1002/cne.10983
55. Stil, A., Jean-Xavier, C., Liabeuf, S., Brocard, C., Delpire, E., Vinay, L., et al. (2011). Contribution of the potassium-chloride co-transporter KCC2 to the modulation of lumbar spinal networks in mice. Eur. J. Neurosci. 33, 1212-1222. doi: 10.1111/j.1460-9568.2010.07592.x
56. Tsujino, H., Kondo, E., Fukuoka, T., Dai, Y., Tokunaga, A., Miki, K., et al. (2000). Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol. Cell. Neurosci. 15, 170-182. doi: 10.1006/mcne.1999.0814
57. Ulmann, L., Hatcher, J. P., Hughes, J. P., Chaumont, S., Green, P. J., Conquet, F., et al. (2008). Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J. Neurosci. 28, 11263-11268. doi: 10.1523/JNEUROSCI.2308-08.2008
58. Valero-Cabré, A., and Navarro, X. (2001). H reflex restitution and facilitation after different types of peripheral nerve injury and repair. Brain Res. 919, 302-312. doi: 10.1016/S0006-8993(01)03052-9
59. Vlug, A. S., Teuling, E., Haasdijk, E. D., French, P., Hoogenraad, C. C., and Jaarsma, D. (2005). ATF3 expression precedes death of spinal motoneurons in amyotrophic lateral sclerosis-SOD1 transgenic mice and correlates with c-Jun phosphorylation, CHOP expression, somato-dendritic ubiquitination and Golgi fragmentation. Eur. J. Neurosci. 22, 1881-1894. doi: 10.1111/j.1460-9568.2005.04389.x
60. Wang, C., Shimizu-Okabe, C., Watanabe, K., Okabe, A., Matsuzaki, H., Ogawa, T., et al. (2002). Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Dev. Brain Res. 139, 59-66. doi: 10.1016/S0165-3806(02)00536-9
61. Wijesekera, L. C., and Leigh, P. N. (2009). Amyotrophic lateral sclerosis. Orphan. J. Rare Dis. 4, 3. doi: 10.1186/1750-1172-4-3