Calcium-activated chloride current expression in axotomized sensory neurons: What for?

Frontiers in Molecular Neuroscience

Volumn , Issue MARCH, 2012, Pages

  Boudes, Mathieu ^a,b,c   Scamps, Frédérique ^a  

^a HÔPITAL SAINT ELOI   (France)

^b LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Axotomy; Bestrophin; CaCC; DRG; Electrical activity; Membrane tension; Regeneration

Indexed keywords

BESTROPHIN 1; CALCIUM ION; CELL PROTEIN; CHLORIDE; NEUROMODULIN; POTASSIUM ION; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ARTICLE; ATOMIC FORCE MICROSCOPY; BEST1 GENE; CALCIUM ACTIVATED CHLORIDE CURRENT; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CELL SWELLING; CHLORIDE CURRENT; GENE; GENE EXPRESSION REGULATION; GENETIC SCREENING; HUMAN; MECHANORECEPTOR; MECHANOTRANSDUCTION; MEDIATOR RELEASE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE FIBER GROWTH; NERVE FIBER TRANSECTION; NERVE REGENERATION; NEURALGIA; NOCICEPTIVE RECEPTOR; NONHUMAN; PERIPHERAL NERVE INJURY; POTASSIUM CURRENT; PROPRIOCEPTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; RNA INTERFERENCE; SENSORY NERVE CELL; SURFACE PROPERTY; TMEM16A GENE;

EID: 84857936369     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2012.00035     Document Type: Article

References (59)

1. Alessandri-Haber, N., Yeh, J. J., Boyd, A. E., Parada, C. A., Chen, X., Reichling, D. B., and Levine, J. D. (2003). Hypotonicity induces TRPV4-mediated nociception in rat. Neuron 39, 497-511.
2. Al-Jumaily, M., Kozlenkov, A., Mechaly, I., Fichard, A., Matha, V., Scamps, F., Valmier, J., and Carroll, P. (2007). Expression of three distinct families of calcium-activated chloride channel genes in the mouse dorsal root ganglion. Neurosci Bull 23, 293-299.
3. Alvarez-Leefmans, F. J., Gamino, S. M., Giraldez, F., and Nogueron, I. (1988). Intracellular chloride regulation in amphibian dorsal root ganglion neurones studied with ionselective microelectrodes. J Physiol 406, 225-246.
4. Andre, S., Boukhaddaoui, H., Campo, B., Al-Jumaily, M., Mayeux, V., Greuet, D., Valmier, J., and Scamps, F. (2003). Axotomy-induced expression of calcium-activated chloride current in subpopulations of mouse dorsal root ganglion neurons. J Neurophysiol 90, 3764-3773.
5. Araki, T., Nagarajan, R., and Milbrandt, J. (2001). Identification of genes induced in peripheral nerve after injury. Expression profiling and novel gene 315 discovery. J Biol Chem 276, 34131-34141.
6. Baptista, A. F., Gomes, J. R., Oliveira, J. T., Santos, S. M., Vannier-Santos, M. A., and Martinez, A. M. (2007). A new approach to assess function after sciatic nerve lesion in the mouse - adaptation of the sciatic static index. J Neurosci Methods 161, 259-264.
7. +-activated Cl-current during development of quail sensory neurons. Dev Biol 136, 129-139.
8. Boudes, M., Pieraut, S., Valmier, J., Carroll, P., and Scamps, F. (2008). Single-cell electroporation of adult sensory neurons for gene screening with RNA interference mechanism. J Neurosci Methods 170, 204-211.
9. +-activated Cl- current expression in axotomized sensory neurons. J Neurosc 29, 10063-10071.
10. Bregestovski, P., Waseem, T., and Mukhtarov, M. (2009). Genetically encoded optical sensors for monitoring of intracellular chloride and chloride-selective channel activity. Front Mol Neurosci 2, 15.
11. Caprini, M., Gomis, A., Cabedo, H., Planells-Cases, R., Belmonte, C., Viana, F., and Ferrer- Montiel, A. (2003). GAP43 stimulates inositol trisphosphate-mediated calcium release in response to hypotonicity. Embo J 22, 3004-3014.
12. Caputo, A., Caci, E., Ferrera, L., Pedemonte, N., Barsanti, C., Sondo, E., Pfeffer, U., Ravazzolo, R., Zegarra-Moran, O., and Galietta, L. J. (2008). TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 322, 590-594.
13. Chien, L. T., and Hartzell, H. C. (2007). Drosophila bestrophin-1 chloride current is dually regulated by calcium and cell volume. J Gen Physiol 130, 513-524.
14. Chien, L. T., and Hartzell, H. C. (2008). Rescue of volume-regulated anion current by bestrophin mutants with altered charge selectivity. J Gen Physiol 132, 537-546.
15. Chub, N., Mentis, G. Z., and O'Donovan M. J. (2006). Chloride-sensitive MEQ fluorescence in chick embryo motoneurons following manipulations of chloride and during spontaneous network activity. J Neurophysiol 95, 323-330.
16. Costigan, M., Befort, K., Karchewski, L., Griffin, R. S., D'Urso, D., Allchorne, A., Sitarski, J., Mannion, J. W., Pratt, R. E., and Woolf, C. J. (2002). Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 3, 16.
17. Currie, K. P., and Scott, R. H. (1992). Calcium-activated currents in cultured neurones from rat dorsal root ganglia. Br J Pharmacol 106, 593-602.
18. de Medinaceli, L. (1995). Interpreting nerve morphometry data after experimental traumatic lesions. J Neurosci Methods 58, 29-37.
19. Duran, C., Thompson, C. H., Xiao, Q., and Hartzell, H. C. (2010). Chloride channels: often enigmatic, rarely predictable. Annu Rev Physiol 72, 95-121.
20. Enes, J., Langwieser, N., Ruschel, J., Carballosa-Gonzalez, M. M., Klug, A., Traut, M. H., Ylera, B., Tahirovic, S., Hofmann, F., Stein, V., Moosmang, S., Hentall, I. D., and Bradke, F. (2010). Electrical activity suppresses axon growth through Ca(v)1.2 channels in adult primary sensory neurons. Curr Biol 20, 1154-1164
21. Geiger, B., Spatz, J. P., and Bershadsky, A. D. (2009). Environmental sensing through focal adhesions. Nat Rev Mol Cell Biol 10, 21-33.
22. + signals in Merkel cells. PLoS One 3, e1750.
23. Hartzell, C., Putzier, I., and Arreola, J. (2005). Calcium-activated chloride channels. Annu Rev Physiol 67, 719-758.
24. (+) current regulates calcium-activated chloride current-induced after depolarization in axotomized sensory neurons. Eur J Neurosci 22, 1073-1080.
25. Hilaire, C., Inquimbert, P., Al-Jumaily, M., Greuet, D., Valmier, J., and Scamps, F. (2005b). Calcium dependence of axotomized sensory neurons excitability. Neurosci Lett 380, 330-334.
26. Hoffmann, E. K., Lambert, I. H., and Pedersen, S. F. (2009). Physiology of cell volume regulation in vertebrates. Physiol Rev 89, 193-277.
27. Hussy, N. (1991). Developmental change in calcium-activated chloride current during the differentiation of Xenopus spinal neurons in culture. Dev Biol 147, 225-238.
28. Hussy, N. (1992). Calcium-activated chloride channels in cultured embryonic Xenopus spinal neurons. J Neurophysiol 68, 2042-2050.
29. Jacob, J. M., and McQuarrie, I. G. (1993). Acceleration of axonal outgrowth in rat sciatic nerve at one week after axotomy. J Neurobiol 24, 356-367.
30. Kalous, A., and Keast, J. R. (2010). Conditioning lesions enhance growth state only in sensory neurons lacking calcitonin gene-related peptide and isolectin B4-binding. Neuroscience 166, 107-121.
31. + -activated Cl- channels bestrophin and anoctamin in epithelial cells. Biol Chem 392, 125-134.
32. Lancaster, E., Oh, E. J., Gover, T., and Weinreich, D. (2002). Calcium and calcium-activated currents in vagotomized rat primary vagal afferent neurons. J Physiol 540, 543-556.
33. Lankford, K. L., Waxman, S. G., and Kocsis, J. D. (1998). Mechanisms of enhancement of neurite regeneration in vitro following a conditioning sciatic nerve lesion. J Comp Neurol 391, 11-29.
34. Leclere, P. G., Norman, E., Groutsi, F., Coffin, R., Mayer, U., Pizzey, J., and Tonge, D. (2007). Impaired axonal regeneration by isolectin B4-binding dorsal root ganglion neurons in vitro. J Neurosc 27, 1190-1199.
35. +-activated Cl- channels. J Clin Invest 120, 1240-1252.
36. Makwana, M., and Raivich, G. (2005). Molecular mechanisms in successful peripheral regeneration. Febs J 272, 2628-2638.
37. Mechaly, I., Bourane, S., Piquemal, D., Al-Jumaily, M., Venteo, S., Puech, S., Scamps, F., Valmier, J., and Carroll, P. (2006). Gene profiling during development and after a peripheral nerve traumatism reveals genes specifically induced by injury in dorsal root ganglia. Mol Cell Neurosci 32, 217-229.
38. Nabekura, J., Ueno, T., Okabe, A., Furuta, A., Iwaki, T., Shimizu-Okabe, C., Fukuda, A., and Akaike, N. (2002). Reduction of KCC2 expression and GABAA receptor-mediated excitation after in vivo axonal injury. J Neurosc 22, 4412-4417.
39. O'Neill, W. C. (1999). Physiological significance of volume-regulatory 410 transporters. Am J Physiol 276, C995-C1011.
40. Pauli, B. U., Abdel-Ghany, M., Cheng, H. C., Gruber, A. D., Archibald, H. A., and Elble, R. C. (2000). Molecular characteristics and functional diversity of CLCA family members. Clin Exp Pharmacol Physiol 27, 901-905.
41. Pfenninger, K. H. (2009). Plasma membrane expansion: a neuron's Herculean task. Nat Rev Neurosci 10, 251-261.
42. Pieraut, S., Lucas, O., Sangari, S., Sar, C., Boudes, M., Bouffi, C., Noel, D., and Scamps, F. (2011). An autocrine neuronal interleukin-6 loop mediates chloride accumulation and NKCC1 phosphorylation in axotomized sensory neurons. J Neurosc 31, 13516-13526.
43. Pieraut, S., Laurent-Matha, V., Sar, C., Hubert, T., Mechaly, I., Hilaire, C., Mersel, M., Delpire, E., Valmier, J., and Scamps, F. (2007). NKCC1 phosphorylation stimulates neurite growth of injured adult sensory neurons. J Neurosc 27, 6751-6759.
44. Raucher, D., and Sheetz, M. P. (2000). Cell spreading and lamellipodial extension rate is regulated by membrane tension. J Cell Biol 148, 127-136.
45. Represa, A., and Ben-Ari, Y. (2005). Trophic actions of GABA on neuronal development. Trends Neurosci 28, 278-283.
46. Ricci, D., Grattarola, M., and Tedesco, M. (2011). The growth cones of living neurons probed by the atomic force microscope. Methods Mol Biol 736, 243-257.
47. Sanchez-Vives, M. V., and Gallego, R. (1994). Calcium-dependent chloride current induced by axotomy in rat sympathetic neurons. J Physiol 475, 391-400.
48. Schroeder, B. C., Cheng, T., Jan, Y. N., and Jan, L. Y. (2008). Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134, 1019-1029.
49. Scott, R. H., Sutton, K. G., Griffin, A., Stapleton, S. R., and Currie, K. P. (1995). Aspects of calcium-activated chloride currents: a neuronal perspective. Pharmacol Ther 66, 535-565.
50. Smith, D. S., and Skene, J. H. (1997). A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth. J Neurosc 17, 646-658.
51. Sun, H., Tsunenari, T., Yau, K. W., and Nathans, J. (2002). The vitelliform macular dystrophy protein defines a new family of chloride channels. Proc Natl Acad Sci U S A 99, 4008-4013.
52. Sung, K. W., Kirby, M., McDonald, M. P., Lovinger, D. M., and Delpire, E. (2000). Abnormal GABAA receptor-mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. J Neurosc 20, 7531-7538.
53. Suzuki, M., and Mizuno, A. (2004). A novel human Cl(-) channel family related to Drosophila flightless locus. J Biol Chem 279, 22461-22468.
54. Tanaka, K., Zhang, Q. L., and Webster, H. D. (1992). Myelinated fiber regeneration after sciatic nerve crush: morphometric observations in young adult and aging mice and the effects of macrophage suppression and conditioning lesions. Exp Neurol 118, 53-61.
55. Viana, F., de la Pena, E., Pecson, B., Schmidt, R. F., and Belmonte, C. (2001). Swelling450 activated calcium signalling in cultured mouse primary sensory neurons. Eur J Neurosci 13, 722-734.
56. Vogelaar, C. F., Vrinten, D. H., Hoekman, M. F., Brakkee, J. H., Burbach, J. P., and Hamers, F. P. (2004). Sciatic nerve regeneration in mice and rats: recovery of sensory innervation is followed by a slowly retreating neuropathic pain-like syndrome. Brain Res 1027, 67-72.
57. Xiao, H. S., Huang, Q. H., Zhang, F. X., Bao, L., Lu, Y. J., Guo, C., Yang, L., Huang, W. J., Fu, G., Xu, S. H., Cheng, X. P., Yan, Q., Zhu, Z. D., Zhang, X., Chen, Z., and Han, Z. G. (2002). Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc Natl Acad Sci U S A 99, 8360-8365.
58. Yang, Y. D., Cho, H., Koo, J. Y., Tak, M. H., Cho, Y., Shim, W. S., Park, S. P., Lee, J., Lee, B., Kim, B. M., Raouf, R., Shin, Y. K., and Oh, U. (2008). TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455, 1210-1215.
59. Zheng, J. Q., and Poo, M. M. (2007). Calcium signaling in neuronal motility. Annu Rev Cell Dev Biol 23, 375-404.