MLC1 protein: A likely link between leukodystrophies and brain channelopathies

Frontiers in Cellular Neuroscience

Volumn 9, Issue APR, 2015, Pages

  Brignone, Maria S ^a   Lanciotti, Angela ^a   Camerini, Serena ^a   De Nuccio, Chiara ^a   Petrucci, Tamara C ^a   Visentinand, Sergio ^a   Ambrosini, Elena ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Astrocytes; Brain edema; Calcium; Chloride ions; Myelin vacuolation; Potassium

Indexed keywords

CALCIUM CHANNEL; CELL ADHESION MOLECULE; CHLORIDE CHANNEL; CYCLIC AMP DEPENDENT PROTEIN KINASE; DYSTROGLYCAN; DYSTROPHIN; EXCITATORY AMINO ACID TRANSPORTER 1; GLIALCAM PROTEIN; ION CHANNEL; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MLC1 PROTEIN; PEPTIDES AND PROTEINS; POTASSIUM CHANNEL KV1.1; PROTEIN CCL2; PROTEIN KINASE C; PROTEIN ZO1; SODIUM CHANNEL; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 4; VOLTAGE DEPENDENT ANION CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL;

ANION TRANSPORT; ARTICLE; ASTROCYTE; BRAIN CHANNELOPATHY; BRAIN DISEASE; CELLULAR DISTRIBUTION; CHLORIDE CURRENT; DOWN REGULATION; GENE MUTATION; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; LEUKODYSTROPHY; LEUKOENCEPHALOPATHY; MEGALENCEPHALIC LEUKOENCEPHALOPATHY; MOLECULAR INTERACTION; NONHUMAN; OSMOREGULATION; PH; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

EID: 84927657153     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00106     Document Type: Article

References (103)

1. Ambrosini, E., Serafini, B., Lanciotti, A., Tosini, F., Scialpi, F., Psaila, R., et al. (2008). Biochemical characterization of MLC1 protein in astrocytes and its association with the dystrophin-glycoprotein complex. Mol. Cell Neurosci. 37, 480-493. doi: 10.1016/j.mcn.2007.11.003
2. Arnedo, T., Aiello, C., Jeworutzki, E., Dentici, M. L., Uziel, G., Simonati, A., et al. (2014a). Expanding the spectrum of megalencephalic leukoencephalopathy with subcortical cysts in two patients with GLIALCAM mutations. Neurogenetics 15, 41-48. doi: 10.1007/s10048-013-0381-x
3. Arnedo, T., López-Hernández, T., Jeworutzki, E., Capdevila-Nortes, X., Sirisi, S., Pusch, M., et al. (2014b). Functional analyses of mutations in HEPACAM causing megalencephalic leukoencephalopathy. Hum. Mutat. 35, 1175-1178. doi: 10.1002/humu.22622
4. Babcock, J. J., and Li, M. (2013). Inside job: ligand-receptor pharmacology beneath the plasma membrane. Acta Pharmacol. Sin. 34, 859-869. doi: 10.1038/aps.2013.51
5. Ballanyi, K., Grafe, P., and Ten Bruggencate, G. (1987). Ion activities and potassium uptake mechanisms of glial cells in guinea-pig olfactory cortex slices. J. Physiol. 382, 159-174. doi: 10.1113/jphysiol.1987.sp016361
6. Barlowe, C. (2003). Signals for COPII-dependent export from the ER: what's the ticket out? Trends Cell Biol. 13, 295-300. doi: 10.1016/S0962-8924(03)00082-5
7. Barrallo-Gimeno, A., and Estévez, R. (2014). GlialCAM, a glial cell adhesion molecule implicated in neurological disease. Adv. Neurobiol. 8, 47-59. doi: 10.1007/978-1-4614-8090-7_3
8. Benfenati, V., Amiry-Moghaddam, M., Caprini, M., Mylonakou, M. N., Rapisarda, C., Ottersen, O. P., et al. (2007). Expression and functional characterization of transient receptor potential vanilloid-related channel 4 (TRPV4) in rat cortical astrocytes. Neuroscience 148, 876-892. doi: 10.1016/j.neuroscience.2007.06.039
9. Benfenati, V., Caprini, M., Dovizio, M., Mylonakou, M. N., Ferroni, S., Ottersen, O. P., et al. (2011). An aquaporin-4/transient receptor potential vanilloid 4 (AQP4/TRPV4) complex is essential for cellvolume control in astrocytes,Proc. Natl. Acad. Sci. U.S.A. 108, 2563-2568. doi: 10.1073/pnas.1012867108
10. Ben-Zeev, B., Levy-Nissenbaum, E., Lahat, H., Anikster, Y., Shinar, Y., Brand, N., et al. (2002). Megalencephalic leukoencephalopathy with subcortical cysts; a founder effect in Israeli patients and a higher than expected carrier rate among. Libyan Jews. Hum. Genet. 111, 214-218. doi: 10.1007/s00439-002-0770-y
11. Blanz, J., Schweizer, M., Auberson, M., Maier, H., Muenscher, A., Hübner, C. A., et al. (2007). Leukoencephalopathy upon disruption of the chloride channel ClC-2. J. Neurosci. 27, 6581-6589. doi: 10.1523/JNEUROSCI.0338-07.2007
12. Bonkowsky, J. L., Nelson, C., Kingston, J. L., Filloux, F. M., Mundorff, M. B., and Srivastava, R. (2010). The burden of inherited leukodystrophies in children. Neurology 75, 718-725. doi: 10.1212/WNL.0b013e3181eee46b
13. Boor, I., Nagtegaal, M., Kamphorst, W., van der Valk, P., Pronk, J. C., van Horssen, J., et al. (2007). MLC1 is associated with the dystrophin-glycoprotein complex at astrocytic endfeet. Acta Neuropathol. 114, 403-410. doi: 10.1007/s00401-007-0247-0
14. Boor, I. P. K., de Groot, K., Mejaski-Bosnjak, V., Brenner, C., van der Knaap, M. S., Scheper, G. C., et al. (2006). Megalencephalic leukoencephalopathy with subcortical cysts: an update and extended mutation analysis of MLC1. Hum. Mutat. 27, 505-512. doi: 10.1002/humu.20332
15. Boor, P. K., de Groot, K., Waisfisz, Q., Kamphorst, W., Oudejans, C. B., Powers, J. M., et al. (2005). MLC1 a novel protein in distal astroglial processes, J. Neuropathol. Exp. Neurol. 64, 412-419.
16. Brignone, M. S., Lanciotti, A., Macioce, P., Macchia, G., Gaetani, M., Aloisi, F., et al. (2011). The beta1 subunit of the Na,K-ATPase pump interacts with megalencephalic leukoencephalopathy with subcortical cysts protein 1 in brain astrocytes: new insights into MLC pathogenesis, Hum. Mol. Gen. 20, 90-103. doi: 10.1093/hmg/ddq435
17. Brignone, M. S., Lanciotti, A., Visentin, S., De Nuccio, C., Molinari, P., Camerini, S., et al. (2014). Megalencephalic leukoencephalopathy with subcortical cysts protein-1 modulates endosomal pH and protein trafficking in astrocytes: relevance to MLC disease pathogenesis. Neurobiol. Dis. 66, 1-18. doi: 10.1016/j.nbd.2014.02.003
18. Brown, D. A. (2006). Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology (Bethesda) 21, 430-439. doi: 10.1152/physiol.00032.2006
19. Bugiani, M., Moroni, I., Bizzi, A., Nardocci, N., Bettecken, T., Gartner, J., et al. (2003). Consciousness disturbances in megalencephalic leukoencephalopathy with subcortical cysts. Neuropediatrics 34, 211-212. doi: 10.1055/s-2003-42209
20. Capdevila-Nortes, X., López-Hernández, T., Apaja, P. M., López de Heredia, M., Sirisi, S., Callejo, G., et al. (2013). Insights into MLC pathogenesis: GlialCAM is an MLC1 chaperone required for proper activation of volume-regulated anion currents. Hum. Mol. Genet. 22, 4405-4416. doi: 10.1093/hmg/ddt290
21. Chang, S. Y., Di, A., Naren, A. P., Palfrey, H. C., Kirk, K. L., and Nelson, D. J. (2002). Mechanisms of CFTR regulation by syntaxin 1A and PKA. J. Cell Sci. 115(Pt 4), 783-791.
22. Christensen, A. P., and Corey, D. P. (2007). TRP channels in mechanosensation: direct or indirect activation? Nat. Rev. Neurosci. 8, 510-521. doi: 10.1038/nrn2149
23. Curran, J., and Mohler, P. J. (2014). Alternative paradigms for ion channelopathies: disorders of ion channel membrane trafficking and posttranslational modification. Annu. Rev. Physiol. 77, 505-524. doi: 10.1146/annurev-physiol-021014-071838
24. Clemente, D., Ortega, M. C., Melero-Jerez, C., and de Castro, F. (2013). The effect of glia-glia interactions on oligodendrocyte precursor cell biology during development and in demyelinating diseases. Front. Cell Neurosci. 7:268. doi: 10.3389/fncel.2013.00268
25. Dart, C. (2010). Lipid microdomains and the regulation of ion channel function. J. Physiol. 588(Pt 17), 3169-3178. doi: 10.1113/jphysiol.2010.191585
26. Depienne, C., Bugiani, M., Dupuits, C., Galanaud, D., Touitou, V., Postma, N., et al. (2013). Brain white matter oedema due to ClC-2 chloride channel deficiency: an observational analytical study. Lancet Neurol. 12, 659-668. doi: 10.1016/S1474-4422(13)70053-X
27. Duarri, A., Lopez de Heredia, M., Capdevila-Nortes, X., Ridder, M. C., Montolio, M., López-Hernández, T., et al. (2011). Knockdown of MLC1 in primary astrocytes causes cell vacuolation: a MLC disease cell model. Neurobiol. Dis. 43, 228-238. doi: 10.1016/j.nbd.2011.03.015
28. Duarri, A., Teijido, O., López-Hernández, T., Scheper, G. C., Barriere, H., Boor, I., et al. (2008). Molecular pathogenesis of megalencephalic leukoencephalopathy with subcortical cysts: mutations in MLC1 cause folding defects. Hum. Mol. Genet. 17, 3728-3739. doi: 10.1093/hmg/ddn269
29. Dubey, M., Bugiani, M., Ridder, M. C., Postma, N. L., Brouwers, E., Polder, E., et al. (2015). Mice with megalencephalic leukoencephalopathy with cysts: a developmental angle. Ann. Neurol. 77, 114-131. doi: 10.1002/ana.24307
30. Farhan, H., Wendeler, M. W., Mitrovic, S., Fava, E., Silberberg, Y., Sharan, R., et al. (2010). MAPK signaling to the early secretory pathway revealed by kinase/phosphatase functional screening. J. Cell Biol. 189, 997-1011. doi: 10.1083/jcb.200912082
31. Florence, C. M., Baillie, L. D., and Mulligan, S. J. (2012). Dynamic volume changes in astrocytes are an intrinsic phenomenon mediated by bicarbonate ion flux. PLoS ONE 7:e51124. doi: 10.1371/journal.pone.0051124
32. González, M. I., Krizman-Genda, E., and Robinson, M. B. (2007). Caveolin-1 regulates the delivery and endocytosis of the glutamate transporter, excitatory amino acid carrier 1. J. Biol. Chem. 282, 29855-29865. doi: 10.1074/jbc.M704738200
33. Gouras, G. K. (2013). Convergence of synapses, endosomes, and prions in the biology of neurodegenerative diseases. Int. J. Cell Biol. 2013, 141083. doi: 10.1155/2013/141083
34. Grant, B. D., and Donaldson, J. G. (2009). Pathways and mechanisms of endocytic recycling. Nat. Rev. Mol. Cell Biol. 10, 597-608. doi: 10.1038/nrm2755
35. Haug, K., Warnstedt, M., Alekov, A. K., Sander, T., Ramírez, A., Poser, B., et al. (2003). Mutations in CLCN2 encoding a voltage-gated chloride channel are associated with idiopathic generalized epilepsies. Nat. Genet. 33, 527-532. doi: 10.1038/ng1121
36. Hoegg-Beiler, M. B., Sirisi, S., Orozco, I. J., Ferrer, I., Hohensee, S., Auberson, M., et al. (2014). Disrupting MLC1 and GlialCAM and ClC-2 interactions in leukodystrophy entails glial chloride channel dysfunction. Nat. Commun. 5, 3475. doi: 10.1038/ncomms4475
37. Hyzinski-García, M. C., Rudkouskaya, A., and Mongin, A. A. (2014). LRRC8A protein is indispensable for swelling-activated and ATP-induced release of excitatory amino acids in rat astrocytes. J. Physiol. 592(Pt 22), 4855-4862. doi: 10.1113/jphysiol.2014.278887
38. Jentsch, T. J., Stein, V., Weinreich, F., and Zdebik, A. A. (2002). Molecular structure and physiological function of chloride channels. Physiol. Rev. 82, 503-68.
39. Jeworutzki, E., Lagostena, L., Elorza-Vidal, X., Lopez-Hernandez, T., Estévez, R., and Pusch, M. (2014). GlialCAM, a CLC-2 Cl(-) channel subunit, activates the slow gate of CLC chloride channels. Biophys. J. 107, 1105-1116. doi: 10.1016/j.bpj.2014.07.040
40. Jeworutzki, E., López-Hernández, T., Capdevila-Nortes, X., Sirisi, S., Bengtsson, L., Montolio, M., et al. (2012). GlialCAM A protein defective in a leukodystrophy, serves as a ClC-2 Cl(-) channel auxiliary subunit. Neuron 73, 951-961. doi: 10.1016/j.neuron.2011.12.039
41. Kim, J. B. (2014). Channelopathies. Korean J. Pediatr. 57, 1-18. doi: 10.3345/kjp.2014.57.1.1
42. Kondapalli, K. C., Prasad, H., and Rao, R. (2014). An inside job: how endosomal Na(+)/H(+) exchangers link to autism and neurological disease. Front. Cell Neurosci. 8:172. doi: 10.3389/fncel.2014.00172
43. Kristensen, B., Birkelund, S., and Jorgensen, P. L. (2003). Trafficking of Na, K-ATPase fused to enhanced green fluorescent protein is mediated by protein kinase A or C. J. Membr. Biol. 191, 25-36. doi: 10.1007/s00232-002-1043-3
44. Lanciotti, A., Brignone, M. S., Bertini, E., Petrucci, T. C., Aloisi, F., and Ambrosini, E. (2013). Astrocytes: emerging stars in leukodystrophy pathogenesis. Transl. Neurosci. 4, 12. doi: 10.2478/s13380-013-0118-1
45. Lanciotti, A., Brignone, M. S., Camerini, S., Serafini, B., Macchia, G., Raggi, C., et al. (2010). MLC1 trafficking and membrane expression in astrocytes: role of caveolin-1 and phosphorylation. Neurobiol. Dis. 37, 581-595. doi: 10.1016/j.nbd.2009.11.008
46. Lanciotti, A., Brignone, M. S., Molinari, P., Visentin, S., De Nuccio, C., Macchia, G., et al. (2012). Megalencephalic leukoencephalopathy with subcortical cysts protein 1 functionally cooperates with the TRPV4 cation channel to activate the response of astrocytes to osmotic stress: dysregulation by pathological mutations. Hum. Mol. Genet. 21, 2166-2180. doi: 10.1093/hmg/dds032
47. Leegwater, P. A., Yuan, B. Q., Van Der Steen, J., Mulders, J., Konst, A. A., Boor, P. K., et al. (2001). Mutations of MLC1 (KIAA0027), encoding a putative membrane protein, cause megalencephalic leukoencephalopathy with subcortical cysts. Am. J. Hum. Genet. 68, 831-838. doi: 10.1086/319519
48. López-Hernández, T., Ridder, M. C., Montolio, M., Capdevila-Nortes, X., Polder, E., Sirisi, S., et al. (2011a). Mutant GlialCAM causes megalencephalic leukoencephalopathy with subcortical cysts, benign familial macrocephaly, and macrocephaly with retardation and autism. Am. J. Hum. Genet. 88, 422-432. doi: 10.1016/j.ajhg.2011.02.009
49. López-Hernández, T., Sirisi, S., Capdevila-Nortes, X., Montolio, M., Fernández-Dueñas, V., Scheper, G. C., et al. (2011b). Molecular mechanisms of MLC1 and GLIALCAM mutations in megalencephalic leukoencephalopathy with subcortical cysts. Hum. Mol. Genet. 20, 3266-3277. doi: 10.1093/hmg/ddr238
50. Mamenko, M., Zaika, O. L., Boukelmoune, N., Berrout, J., O'Neil, R. G., and Pochynyuk, O. (2013). Discrete control of TRPV4 channel function in the distal nephron by protein kinases A and C. J. Biol. Chem. 88, 20306-20314. doi: 10.1074/jbc.M113.466797
51. Masaki, K., Suzuki, S. O., Matsushita, T., Yonekawa, T., Matsuoka, T., Isobe, N., et al. (2012). Extensive loss of connexins in Baló's disease: evidence for an auto-antibody-independent astrocytopathy via impaired astrocyte-oligodendrocyte/myelin interaction. Acta Neuropathol. 123, 887-900. doi: 10.1007/s00401-012-0972-x
52. Mejaski-Bosnjak, V., Besenski, N., Brockmann, K., Pouwels, P. J., Frahm, J., and Hanefeld, F. A. (1997). Cystic leukoencephalopathy in a megalencephalic child: clinical and magnetic resonance imaging/magnetic resonance spectroscopy findings. Pediatr. Neurol. 16, 347-350. doi: 10.1016/S0887-8994(97)00044-1
53. Meyer, J., Huberth, A., Ortega, G., Syagailo, Y. V., Jatzke, S., Mössner, R., et al. (2001). A missense mutation in a novel gene encoding a putative cation channel is associated with catatonic schizophrenia in a large pedigree. Mol. Psychiatry 6, 302-306. doi: 10.1038/sj.mp.4000869
54. Michelsen, K., Yuan, H., and Schwappach, B. (2005). Hide and run. Arginine-based endoplasmic-reticulum-sorting motifs in the assembly of heteromultimeric membrane proteins. EMBO Rep. 6, 717-22. doi: 10.1038/sj.embor.7400480
55. Molofsky, A. V., Krencik, R., Ullian, E. M., Tsai, H. H., Deneen, B., Richardson, W. D., et al. (2012). Astrocytes and disease: a neurodevelopmental perspective. Genes Dev. 26, 891-907. doi: 10.1101/gad.188326.112
56. Montagna, G., Teijido, O., Eymard-Pierre, E., Muraki, K., Cohen, B., Loizzo, A., et al. (2006). Vacuolating megalencephalic leukoencephalopathy with subcortical cysts: functional studies of novel variants in MLC1. Hum. Mutat. 27, 292. doi: 10.1002/humu.9407
57. Neusch, C., Rozengurt, N., Jacobs, R. E., Lester, H. A., and Kofuji, P. (2001). Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. J. Neurosci. 21, 5429-5438.
58. Nico, B., Frigeri, A., Nicchia, G. P., Corsi, P., Ribatti, D., Quondamatteo, F., et al. (2003). Severe alterations of endothelial and glial cells in the blood-brain barrier of dystrophic mdx mice. Glia 42, 235-251. doi: 10.1002/glia.10216
59. Nico, B., Paola Nicchia, G., Frigeri, A., Corsi, P., Mangieri, D., Ribatti, D., et al. (2004). Altered blood-brain barrier development in dystrophic MDX mice. Neuroscience 125, 921-935. doi: 10.1016/j.neuroscience.2004.02.008
60. Nilius, B., and Voets, T. (2013). The puzzle of TRPV4 channelopathies. EMBO Rep. 14, 152-163. doi: 10.1038/embor.2012.219
61. Noël, G., Belda, M., Guadagno, E., Micoud, J., Klöcker, N., and Moukhles, H. (2005). Dystroglycan and Kir4.1 coclustering in retinal Müller glia is regulated by laminin-1 and requires the PDZ-ligand domain of Kir4.1. J Neurochem. 94, 691-702. doi: 10.1111/j.1471-4159.2005.03191.x
62. Noell, S., Wolburg-Buchholz, K., Mack, A. F., Beedle, A. M., Satz, J. S., Campbell, K. P., et al. (2011). Evidence for a role of dystroglycan regulating the membrane architecture of astroglial endfeet. Eur. J. Neurosci. 33, 2179-2186. doi: 10.1111/j.1460-9568.2011.07688.x
63. Okada, Y., Sato, K., and Numata, T. (2009). Pathophysiology and puzzles of the volume-sensitive outwardly rectifying anion channel. J. Physiol. 587(Pt 10), 2141-2149. doi: 10.1113/jphysiol.2008.165076
64. Pascual-Castroviejo, I., van der Knaap, M. S., Pronk, J. C., García-Segura, J. M., Gutiérrez-Molina, M., and Pascual-Pascual, S. I. (2005). Vacuolating megalencephalic leukoencephalopathy: 24 year follow-up of two siblings. Neurologia 20, 33-40.
65. Patrono, C., Di Giacinto, G., Eymard-Pierre, E., Santorelli, F. M., Rodriguez, D., De Stefano, N., et al. (2003). Genetic heterogeneity of megalencephalic leukoencephalopathy and subcortical cysts. Neurology 61, 534-537. doi: 10.1212/01.WNL.0000076184.21183.CA
66. Pedersen, S. F., Klausen, T. K., and Nilius, B. (2015). The identification of VRAC (Volume Regulated Anion Channel): an amazing Odyssey. Acta Physiol. (Oxf) doi: 10.1111/apha.12450 [Epub ahead of print].
67. Petrini, S., Minnone, G., Coccetti, M., Frank, C., Aiello, C., Cutarelli, A., et al. (2013). Monocytes and macrophages as biomarkers for the diagnosis of megalencephalic leukoencephalopathy with subcortical cysts. Mol. Cell Neurosci. 56, 307-321. doi: 10.1016/j.mcn.2013.07.001
68. Pfrieger, F. W. (2009). Roles of glial cells in synapse development. Cell Mol. Life Sci. 66, 662037-2047. doi: 10.1007/s00018-009-0005-7
69. Poole, D. P., Amadesi, S., Veldhuis, N. A., Abogadie, F. C., Lieu, T., Darby, W., et al. (2013). Protease-activated receptor 2 (PAR2) protein and transient receptor potential vanilloid 4 (TRPV4) protein coupling is required for sustained inflammatory signaling. J. Biol. Chem. 288, 5790-5802. doi: 10.1074/jbc.M112.438184
70. Qiu, Z., Dubin, A. E., Mathur, J., Tu, B., Reddy, K., Miraglia, L. J., et al. (2014). SWELL1, a plasma membrane protein, is an essential component of volume-regulated anion channel. Cell 157, 447-458. doi: 10.1016/j.cell.2014.03.024
71. Ridder, M. C., Boor, I., Lodder, J. C., Postma, N. L., Capdevila-Nortes, X., Duarri, A., et al. (2011). Megalencephalic leucoencephalopathy with cysts: defect in chloride currents and cell volume regulation. Brain 134, 3342-3354. doi: 10.1093/brain/awr255
72. Scheper, G. C., van Berkel, C. G., Leisle, L., de Groot, K. E., Errami, A., Jentsch, T. J., et al. (2010). Analysis of CLCN2 as candidate gene for megalencephalic leukoencephalopathy with subcortical cysts. Genet. Test Mol. Biomarkers 14, 225-257. doi: 10.1089/gtmb.2009.0148
73. Schmitt, A., Gofferje, V., Weber, M., Meyer, J., Mössner, R., and Lesch, K. P. (2003). The brainspecific protein MLC1 implicated in megalencephalic leukoencephalopathy with subcortical cysts is expressed in glial cells in the murine brain. Glia 44, 283-295. doi: 10.1002/glia.10304
74. Schutze, M. P., Peterson, P. A., and Jackson, M. R. (1994). An N-terminal double-arginine motif maintains type II membrane proteins in the endoplasmic reticulum. EMBO J. 13, 1696-1705.
75. Scott, C. C., and Gruenberg, J. (2011). Ion flux and the function of endosomes and lysosomes: pH is just the start: the flux of ions across endosomal membranes influences endosome function not only through regulation of the luminal pH. Bioessays 33, 103-110. doi: 10.1002/bies.201000108
76. Scott, D. B., Blanpied, T. A., and Ehlers, M. D. (2003). Coordinated PKA and PKC phosphorylation suppresses RXR-mediated ER retention and regulates the surface delivery of NMDA receptors. Neuropharmacology 45, 755-767. doi: 10.1016/S0028-3908(03)00250-8
77. Shikano, S., and Li, M. (2003). Membrane receptor trafficking: evidence of proximal and distal zones conferred by two independent endoplasmic reticulum localization signals. Proc. Natl. Acad. Sci. U.S.A. 100, 5783-5788. doi: 10.1073/pnas.1031748100
78. Simons, K., and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572. doi: 10.1038/42408
79. Singhal, B. S., Gorospe, J. R., and Naidu, S. (2003). Megalencephalic leukoencephalopathy with subcortical cysts. J. Child Neurol. 18, 646-652. doi: 10.1177/08830738030180091201
80. Singhal, B. S., Gursahani, R. D., Udani, V. P., and Biniwale, A. A. (1996). Megalencephalic leukodystrophy in an Asian Indian ethnic group. Pediatr. Neurol. 14, 291-296. doi: 10.1016/0887-8994(96)00048-3
81. Sirisi, S., Folgueira, M., Lopez-Hernandez, T., Minieri, L., Pérez-Rius, C., Gaitán-Peñas, H., et al. (2014). Megalencephalic leukoencephalopathy with subcortical Cysts protein 1 regulates glial surface localization of GLIALCAM from fish to humans. Hum. Mol. Genet. 23, 5069-5086. doi: 10.1093/hmg/ddu231
82. Sivaprasadarao, A., Taneja, T. K., Mankouri, J., and Smith, A. J. (2007). Trafficking of ATP-sensitive potassium channels in health and disease. Biochem. Soc. Trans. 35, 1055-1059. doi: 10.1042/BST0351055
83. Sjö, A., Magnusson, K. E., and Peterson, K. H. (2005). Association of alpha-dystrobrevin with reorganizing tight junctions. J. Membr. Biol. 203, 21-30. doi: 10.1007/s00232-004-0728-1
84. Smith, Q. R., Johnson, C. E., and Woodbury, D. M. (1981). Uptake of 36Cl_ and 22Na by the brain-cerebrospinal fluid system. J. Neurochem. 37, 117-124. doi: 10.1111/j.1471-4159.1981.tb05298.x
85. Son, Y. K., Park, H., Firth, A. L., and Park, W. S. (2013). Side-effects of protein kinase inhibitors on ion channels. J. Biosci. 38, 937-949. doi: 10.1007/s12038-013-9383-y
86. Steinke, V., Meyer, J., Syagailo, Y. V., Ortega, G., Hameister, H., Mössner, R., et al. (2003). The genomic organization of the murine Mlc1 (Wkl1, KIAA0027) gene. J. Neural. Transm. 110, 333-343. doi: 10.1007/s00702-002-0788-2
87. Teijido, O., Martínez, A., Pusch, M., Zorzano, A., Soriano, E., Del Río, J. A., et al. (2004). Localization and functional analyses of the MLC1 protein involved in megalencephalic leukoencephalopathy with subcortical cysts. Hum. Mol. Genet. 13, 2581-2594. doi: 10.1093/hmg/ddh291
88. Topçu, M., Gartioux, C., Ribierre, F., Yalçinkaya, C., Tokus, E., Oztekin, N., et al. (2000). Vacuoliting megalencephalic leukoencephalopathy with subcortical cysts, mapped to chromosome 22qtel. Am. J. Hum. Genet. 66, 733-739. doi: 10.1086/302758
89. Topcu, M., Saatci, I., Topcuoglu, M. A., Kose, G., and Kunak, B. (1998). Megalencephaly and leukodystrophy with mild clinical course: a report on 12 new cases. Brain Dev. 20, 142-153. doi: 10.1016/S0387-7604(98)00002-3
90. Vaknin-Dembinsky, A., Karussis, D., Avichzer, J., and Abramsky, O. (2014). NMO spectrum of disorders: a paradigm for astrocyte-targeting autoimmunity and its implications for MS and other CNS inflammatory diseases. J. Autoimmun. 54, 93-99. doi: 10.1016/j.jaut.2014.05.004
91. Van der Knaap, M. S., Barth, P. G., Stroink, H., van Nieuwenhuizen, O., Arts, W. F., Hoogenraad, F., et al. (1995a). Leukoencephalopathy with swelling and a discrepantly mild clinical course in eight children. Ann. Neurol. 37, 324-334. doi: 10.1002/ana.410370308
92. Van der Knaap, M. S., Valk, J., Barth, P. G., Smit, L. M., van Engelen, B. G., and Tortori Donati, P. (1995b). Leukoencephalopathy with swelling in children and adolescents: MRI patterns and differential diagnosis. Neuroradiology 37, 679-686. doi: 10.1007/BF00593394
93. Van der Knaap, M. S., Barth, P. G., Vrensen, G. F., and Valk, J. (1996). Histopathology of an infantile-onset spongiform leukoencephalopathy with a discrepantly mild clinical course. Acta Neuropathol. 92, 206-212. doi: 10.1007/s004010050510
94. Van der Knaap, M. S., Boor, I., and Estévez, R. (2012). Megalencephalic leukoencephalopathy with subcortical cysts: chronic white matter oedema due to a defect in brain ion and water homoeostasis. Lancet Neurol. 11, 973-985. doi: 10.1016/S1474-4422(12)70192-8
95. Venkatachalam, K., Wong, C. O., and Zhu, M. X. (2014). The role of TRPMLs in endolysosomal trafficking and function. Cell Calcium doi: 10.1016/j.ceca.2014.10.008 [Epub ahead of print].
96. Voss, F. K., Ullrich, F., Münch, J., Lazarow, K., Lutter, D., Mah, N., et al. (2014). Identification of LRRC8 heteromers as an essential component of the volume-regulated anion channel VRAC. Science 344, 634-638. doi: 10.1126/science.1252826
97. Walz, W. (2002). Chloride/anion channels in glial cell membranes. Glia 40, 1-10. doi: 10.1002/glia.10125
98. Wang, X., Matteson, J., An, Y., Moyer, B., Yoo, J. S., Bannykh, S., et al. (2004). COPII-dependent export of cystic fibrosis transmembrane conductance regulator from the ER uses a di-acidic exit code. J. Cell Biol. 167, 65-74. doi: 10.1083/jcb.200401035
99. Wang, X., and Paller, A. S. (2006). Lipid Rafts: membrane Triage Centers. J. Invest. Dermatol. 126, 951-953. doi: 10.1038/sj.jid.5700282
100. Wingerchuk, D. M., Lennon, V. A., Lucchinetti, C. F., Pittock, S. J., and Weinshenker, B. G. (2007). The spectrum of neuromyelitis optica. Lancet Neurol. 6, 805-815. doi: 10.1016/S1474-4422(07)70216-8
101. Xu, H., Zhao, H., Tian, W., Yoshida, K., Roullet, J. B., and Cohen, D. M. (2003). Regulation of a transient receptor potential (TRP) channel by tyrosine phosphorylation. SRC family kinase-dependent tyrosine phosphorylation of TRPV4 on TYR-253 mediates its response to hypotonic stress. J. Biol. Chem. 278, 11520-11527. doi: 10.1074/jbc.M211061200
102. Zhang, X., Dong, C., Wu, Q. J., Balch, W. E., and Wu, G. (2011). Di-acidic motifs in the membrane-distal C termini modulate the transport of angiotensin II receptors from the endoplasmic reticulum to the cell surface. J. Biol. Chem. 286, 20525-20535. doi: 10.1074/jbc.M111.222034
103. Zschocke, J., Bayatti, N., and Behl, C. (2005). Caveolin and GLT-1 gene expression is reciprocally regulated in primary astrocytes: association of GLT-1 with non-caveolar lipid rafts. Glia 49, 275-287. doi: 10.1002/glia.20116