The β1 subunit of the Na, K-ATPase pump interacts with megalencephalic leucoencephalopathy with subcortical cysts protein 1 (MLC1) in brain astrocytes: New insights into MLC pathogenesis

Human Molecular Genetics

Volumn 20, Issue 1, 2011, Pages 90-103

  Brignone, Maria S ^a   Lanciotti, Angela ^a   Macioce, Pompeo ^a   Macchia, Gianfranco ^a   Gaetani, Matteo ^a   Aloisi, Francesca ^a   Petrucci, Tamara C ^a   Ambrosini, Elena ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATASE (POTASSIUM); DYSTROBREVIN; MEMBRANE PROTEIN; MLC1 PROTEIN; SYNTROPHIN; UNCLASSIFIED DRUG; ATP1B1 PROTEIN, HUMAN; MLC1 PROTEIN, HUMAN; MULTIPROTEIN COMPLEX;

AFFINITY CHROMATOGRAPHY; ARTICLE; ASTROCYTE; BRAIN SIZE; BRAIN TISSUE; CONTROLLED STUDY; ENDOSOME; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKOENCEPHALOPATHY; MEGALENCEPHALIC LEUCOENCEPHALOPATHY WITH SUBCORTICAL CYST; NONHUMAN; OSMOSIS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN INTERACTION; YEAST; ANIMAL; BRAIN; CELL CULTURE; CYST; DEMYELINATING DISEASE; GENETICS; METABOLISM; MULTIPLE SCLEROSIS; PATHOLOGY; RAT; WISTAR RAT;

RATTUS; STROPHANTHUS GRATUS;

ANIMALS; ASTROCYTES; BRAIN; CELLS, CULTURED; CYSTS; HEREDITARY CENTRAL NERVOUS SYSTEM DEMYELINATING DISEASES; HUMANS; MEMBRANE PROTEINS; MULTIPLE SCLEROSIS; MULTIPROTEIN COMPLEXES; RATS; RATS, WISTAR; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 79953685240     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq435     Document Type: Article

References (81)

1. Van der Knaap, M.S., Barth, P.G., Stroink, H., Van Nieuwenhuizen, O., Arts, W.F., Hoogenraad, F. and Valk, J. (1995) Leukoncephalopathy with swelling and a discrepantly mild clinical course in eight children. Ann. Neurol., 7, 324-334.
2. Leegwater, P.A., Yuan, B.Q., Van Der Steen, J., Mulders, J., Konst, A.A., Boor, P.K., Mejaski-Bosnjak, V., Van Der Maarel, S.M., Frants, R.R., Oudejans, C.B. 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.
3. Pascual-Castroviejo, I., Van der Knaap, M.S., Pronk, J.C., Garcia-Segura, J.M., Gutierez-Molina, M. and Pascual-Pascual, S.I. (2005) Vacuolating megalencephalic leukoencephalopathy: 24 year follow-up of two siblings. Neurologia, 20, 33-40.
4. Topku, M., Gartioux, C., Ribierre, F.,Yalçinkaya, C., Tokus, E., Oztekin, N., Beckmann, J.S., Ozguc, M. and Seboun, E. (2000) Vacuolating megalencephalic leukoencephalopathy with subcortical cysts mapped to chromosome 22qtel. Am. J. Hum. Genet., 66, 733-739.
5. Boor, P.K.I., de Groot, K., Mejaski-Bosnjak, V., Brenner, C., van der Knaap, M.S., Scheper, G.C. and Pronk, J.C. (2006) Megalencephalic leukoencephalopathy with subcortical cysts: an update and extended mutation analysis of MLC1. Hum. Mutat., 27, 505-512.
6. Blattner, R., Von Moers, A., Leegwater, P.A., Hanefeld, F.A., Van Der Knaap, M.S. and Köhler, W. (2003) Clinical and genetic heterogeneity in megalencephalic leukoencephalopathy with subcortical cysts (MLC). Neuropediatrics, 34, 215-218.
7. Patrono, C., Di Giacinto, G., Eymard-Pierre, E., Santorelli, F.M., Rodriguez, D., De Stefano, N., Federico, A., Gatti, R., Benigno, V., Megarbané, A. et al. (2003) Genetic heterogeneity of megalencephalic leukoencephalopathy and subcortical cysts. Neurology, 61, 534-537.
8. van der Knaap, M.S., Lai, V., Köhler, W., Salih, M.A., Fonseca, M.J., Benke, T.A., Wilson, C., Jayakar, P., Aine, M.R., Dom, L. et al. (2010) Megalencephalic leukoencephalopathy with cysts without MLC1 defect. Ann. Neurol., 67, 834-837.
9. Teijido, O., Martinez, A., Pusch,M., Zorzano, A., Soriano, E., Del Rio, J.A., Palacin, M. and Estevez, R. (2004) Localization and functional analyses of the MLC1 protein involved in megalencephalic leukoencephalopathy with subcortical cysts. Hum. Mol. Genet., 13, 2581-2594.
10. Boor, P.K.I., DeGroot, K.,Waisfisz, Q., Kamphrost, W., Oudejans, C.B.M., Powers, J.M., Pronk, J.C., Shepert, G.C. and Van Der Knaap, M.S. (2005) MLC1 a novel protein in distal astroglial processes. J. Neuropathol. Exp. Neurol., 64, 412-419.
11. Ambrosini, E., Serafini, B., Lanciotti, A., Tosini, F., Scialpi, F., Psaila, R., Di Girolamo, F., Petrucci, T.C. and Aloisi, F. (2008) Biochemical characterization of MLC1 protein in astrocytes and its association with the dystrophin-glycoprotein complex. Mol. Cell. Neurosci., 37, 480-493.
12. Kimelberg, H.K. (2010) Functions of mature mammalian astrocytes: a current view. Neuroscientist, 16, 79-106.
13. Boor, P.K.I., Nagtegaal, M., Kamphorst, W., van der Valk, P., Pronk, J.C., van Horssen, J., Dinopoulos, A., Bove, K.E., Pascual-Castroviejo, I., Muntoni, F. et al. (2007) MLC1 is associated with the dystrophin-glycoprotein complex at astrocytic endfeet. Acta Neuropathol., 114, 403-410.
14. Lanciotti, A., Brignone, M.S., Camerini, S., Serafini, B., Macchia, G., Raggi, C., Molinari, P., Crescenzi, M., Musumeci, M., Sargiacomo, M. et al. (2010) MLC1 trafficking and membrane expression in astrocytes: role of caveolin-1 and phosphorylation. Neurobiol. Dis., 37, 581-595.
15. Waite, A., Tinsley, C.L., Locke, M. and Blake, D.J. (2009) The neurobiology of the dystrophin-associated glycoprotein complex. Ann. Med., 41, 344-359.
16. Neely, J.D., Amiry-Moghaddam, M., Ottersen, O.P., Froehner, S.C., Agre, P. and Adams, M.E. (2001) Syntrophin-dependent expression and localization of Aquaporin-4 water channel protein. Proc. Natl Acad. Sci. USA, 98, 14108-14113.
17. Connors, N.C., Adams, M.E., Froehner, S.C. and Kofuji, P. (2004) The potassium channel Kir4.1 associates with the dystrophin-glycoprotein complex via alpha-syntrophin in glia. J. Biol. Chem., 279, 28387-28392.
18. +-ATPase in cultured rat astrocytes. J. Neurochem., 69, 2189-2196.
19. +-ATPase using a new ouabain-affinity column. Am. J. Physiol., 275, C1167-C1177.
20. Rose, E.M., Koo, J.C., Antflick, J.E., Ahmed, S.M., Angers, S. and Hampson, D.R. (2009) Glutamate transporter coupling to Na,K-ATPase. J. Neurosci., 24, 8143-8155.
21. Amiry-Moghaddam, M., Frydenlund, D.S. and Ottersen, O.P. (2004) Anchoring of aquaporin-4 in brain: molecular mechanisms and implications for the physiology and pathophysiology of water transport. Neuroscience, 129, 999-1010.
22. Illarionova, N.B., Gunnarson, E., Li, Y., Brismar, H., Bondar, A., Zelenin, S. and Aperia, A. (2010) Functional and molecular interactions between aquaporins and Na,K-ATPase. Neuroscience, 168, 915-925.
23. Cain, C.C. and Murphy, R.F. (1988) A chloroquine-resistant Swiss 3T3 cell line with a defect in late endocytic acidification. J. Cell. Biol., 106, 269-277.
24. Lecuona, E., Ridge, K., Pesce, L., Batlle, D. and Sznajder, J.I. (2003) The GTP-binding protein RhoA mediates Na,K-ATPase exocytosis in alveolar epithelial cells. Mol. Biol. Cell., 14, 3888-3897.
25. +-ATPase-containing vesicles in alveolar epithelial cells. J. Cell. Sci., 122, 3915-3922.
26. +-ATPase motion and incorporation into the plasma membrane in response to G protein-coupled receptor signals in living cells. Mol. Biol. Cell., 14, 1149-1157.
27. Olson, J.E., Sankar, R., Holtzman, D., James, A. and Fleischhacker, D. (1986) Energy-dependent volume regulation in primary cultured cerebral astrocytes. J. Cell. Physiol., 128, 209-215.
28. Fraser, C.L. and Swanson, R.A. (1994) Female sex hormones inhibit volume regulation in rat brain astrocyte culture. Am. J. Physiol., 267, C909-C914.
29. Kimelberg, H.K. (1986) Occurrence and functional significance of serotonin and catecholamine uptake by astrocytes. Biochem. Pharmacol., 35, 2273-2281.
30. Kimelberg, H.K. (2004) Volume activated anion channel and astrocytic cellular edema in traumatic brain injury and stroke. Adv. Exp. Med. Biol., 559, 157-167.
31. Chawla, S., Skepper, J.N., Fraser, J.F. and Huang, C.L. (2002) Osmotic processes in vacuolation and detubulation of skeletal muscle. Cell Biol. Int., 26, 905-910.
32. Koffer, A., Williams, M. and Johansen, T. (2002) Vacuole formation in mast cells responding to osmotic stress and to F-actin disassembly. Cell Biol. Int., 26, 885-892.
33. Iwasa, Y., Hirono, C., Sugita, M., Takemoto, K. and Shiba, Y. (2001) External Cl(-)-dependent formation of watery vacuoles by long-term hypotonic shock in 3T3-L1 cells. Cell. Physiol. Biochem., 11, 311-320.
34. +-ATPase in living cells. Proc. Natl Acad. Sci. USA, 86, 544-548.
35. Grabe, M. and Oster, G. (2001) Regulation of organelle acidity. J. Gen. Physiol., 117, 329-344.
36. +-ATPase and cardiac steroids in the regulation of endocytosis. Am. J. Physiol. Cell. Physiol., 293, C885-C896.
37. Cain, C.C. and Murphy, R.F. (1986) Growth inhibition of 3T3 fibroblasts by lysosomotropic amines: correlation with effects on intravesicular pH but not vacuolation. J. Cell. Physiol., 129, 65-70.
38. Wegner, C.S., Malerød, L., Pedersen, N.M., Progida, C., Bakke, O., Stenmark, H. and Brech, A. (2010) Ultrastructural characterization of giant endosomes induced by GTPase-deficient Rab5. Histochem. Cell Biol., 133, 41-55.
39. Gorvel, J.P., Chavrier, P., Zerial, M. and Gruenberg, J. (1991) rab5 controls early endosome fusion in vitro. Cell., 64, 915-925.
40. Gillooly, D.J., Raiborg, C. and Stenmark, H. (2003) Phosphatidylinositol 3-phosphate is found in microdomains of early endosomes. Histochem. Cell. Biol., 120, 445-453.
41. Zerial, M. and McBride, H. (2001) Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol., 2, 107-117.
42. Bucci, C., Parton, R.G., Mather, I.H., Stunnenberg, H., Simons, K., Hoflack, B. and Zerial, M. (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell, 70, 715-728.
43. Henics, T. and Wheatley, D.N. (1997) Vacuolar cytoplasmic phase separation in cultured mammalian cells involves the microfilament network and reduces motional properties of intracellular water. Int. J. Exp. Pathol., 78, 343-354.
44. Kruczek, C., Görg, B., Keitel, V., Pirev, E., Kröncke, K.D., Schliess, F. and Häussinger, D. (2009) Hypoosmotic swelling affects zinc homeostasis in cultured rat astrocytes. Glia, 57, 79-92.
45. Macioce, P., Gambara, G., Bernassola, M., Gaddini, L., Torreri, P., Macchia, G., Ramoni, C., Ceccarini, M. and Petrucci, T.C. (2003) Beta-dystrobrevin interacts directly with kinesin heavy chain in brain. J. Cell Sci., 116, 4847-4856.
46. Neely, J.D., Christensen, B.M., Nielsen, S. and Agre, P. (1999) Heterotetrameric composition of aquaporin-4 water channels. Biochemistry, 38, 11156-11163.
47. +-ATPase. J. Biol. Chem., 279, 17250-17259.
48. Cai, T., Wang, H., Chen, Y., Liu, L., Gunning, W.T., Quintas, L.E. and Xie, Z.J. (2008) Regulation of caveolin-1 membrane trafficking by the Na/K-ATPase. J. Cell Biol., 182, 1153-1169.
49. + homeostasis? Neuron. Glia Biol., 26, 1-9.
50. Sofroniew, M.V. and Vinters, H.V. (2010) Astrocytes: biology and pathology. Acta Neuropathol., 119, 7-35.
51. Kaplan, J.H. (2002) Biochemistry of Na,K-ATPase. Annu. Rev. Biochem., 71, 511-535.
52. Therien, G., Pu, H.X., Karlish, S.J. and Blostein, R. (2001) Molecular and functional studies of the gamma subunit of the sodium pump. J. Bioenerg. Biomembr., 33, 407-414.
53. Gegelashvili, M., Rodriguez-Kern, A., Sung, L., Shimamoto, K. and Gegelashvili, G. (2007) Glutamate transporter GLAST/EAAT1 directs cell surface expression of FXYD2/gamma subunit of Na,K-ATPase in human fetal astrocytes. Neurochem. Int., 50, 916-920.
54. Geering, K. (2008) Functional roles of Na,K-ATPase subunits. Curr. Opin. Nephrol. Hypertens., 17, 526-532.
55. +-ATPase: an indispensable ion pumping-signaling mechanism across mammalian cell membranes. Semin. Nephrol., 26, 386-392.
56. +-ATPase alpha-subunit. Biochim. Biophys. Acta, 1330, 217-224.
57. +-ATPase interacts with BKCa channels and affects their steady-state expression on the cell surface. FEBS Lett., 583, 3109-3114.
58. + channel in the basolateral membrane of renal proximal tubule. J. Gen. Physiol., 111, 161-180.
59. Priebe, L., Friedrich, M. and Benndorf, K. (1996) Functional interaction between K(ATP) channels and the Na(+)-K(+) pump in metabolically inhibited heart cells of the guinea-pig. J. Physiol., 492, 405-417.
60. Mao, H., Ferguson, T.S., Cibulsky, S.M., Holmqvist, M., Ding, C., Fei, H. and Levitan, I.B. (2005) MONaKA, a novel modulator of the plasma membrane Na,K-ATPase. J. Neurosci., 25, 7934-7943.
61. Gorokhova, S., Bibert, S., Geering, K. and Heintz, N. (2007) A novel family of transmembrane proteins interacting with beta subunits of the Na,K-ATPase. Hum. Mol. Genet., 16, 2394-2410.
62. +-ATPase in regulating ATP-dependent endosome acidification. Proc. Natl Acad. Sci. USA, 86, 539-543.
63. +)-ATPase in the brain. Epilepsia, 33, 58-64.
64. Gloor, S., Antonicek, H., Sweadner, K.J., Pagliusi, S., Frank, R., Moos, M. and Schachner, M. (1990) The adhesion molecule on glia (AMOG) is a homologue of the beta subunit of the Na,K-ATPase. J. Cell Biol., 110, 165-174.
65. Benfenati, V. and Ferroni, S. (2010) Water transport between CNS compartments: functional and molecular interactions between aquaporins and ion channels. Neuroscience, 168, 926-940.
66. Friedrich, B., Matskevich, I. and Lang, F. (2006) Cell volume regulatory mechanisms. Contrib. Nephrol., 152, 1-8.
67. Lang, F. (2007) Mechanisms and significance of cell volume regulation. J. Am. Coll. Nutr., 26, 613S-623S.
68. Schneider, G.H., Baethmann, A. and Kempski, O. (1992) Mechanisms of glial swelling induced by glutamate. Can. J. Physiol. Pharmacol., 70, 334-343.
69. Hansson, E. (1994) Metabotropic glutamate receptor activation induces astroglial swelling. J. Biol. Chem., 269, 21955-21961.
70. + influx. J. Neurosci. Res., 52, 307-321.
71. Koyama, Y., Ishibashi, T., Okamoto, T., Matsuda, T., Hashimoto, H. and Baba, A. (2000) Transient treatments with L-glutamate and threo-beta-hydroxyaspartate induce swelling of rat cultured astrocytes. Neurochem. Int., 36, 167-173.
72. + pump alpha-2 subunit expression. Ann. NY Acad. Sci., 986, 509-513.
73. Hartford, A.K., Messer, M.L., Moseley, A.E., Lingrel, J.B. and Delamere, N.A. (2004) Na,K-ATPase alpha 2 inhibition alters calcium responses in optic nerve astrocytes. Glia, 45, 229-237.
74. + ATPase. Dev. Neurosci., 18, 336-342.
75. Magistretti, P.J. (2009) Neuroscience. Low-cost travel in neurons. Science, 325, 1349-1351.
76. Soe, R., Macaulay, N. and Klaerke, D.A. (2009) Modulation of Kir4.1 and Kir4.1-Kir5.1 channels by small changes in cell volume. Neurosci. Lett., 457, 80-84.
77. Hirrlinger, P.G., Wurm, A., Hirrlinger, J., Bringmann, A. and Reichenbach, A. (2008) Osmotic swelling characteristics of glial cells in the murine hippocampus, cerebellum, and retina in situ. J. Neurochem., 105, 1405-1417.
78. Gorospe, J.R. and Maletkovic, J. (2006) Alexander disease and megalencephalic leukoencephalopathy with subcortical cysts: leukodystrophies arising from astrocyte dysfunction. Ment. Retard. Dev. Disabil. Res. Rev., 12, 113-122.
79. Tinsa, F., Farid, O., Douira, W., Rodriguez, D., Burglen, L., Boussetta, K. and Bousnina, S. (2009) Megalencephalic leukoencephalopathy with subcortical cysts in a Tunisian boy. J. Child Neurol., 24, 87-89.
80. Agresti, C., Aloisi, F. and Levi, G. (1991) Heterotypic and homotypic cellular interactions influencing the growth and differentiation of bipotential oligodendrocyte-type-2 astrocyte progenitors in culture. Dev. Biol., 144, 16-29.
81. Kimelberg, H.K. and O'Connor, E. (1988) Swelling of astrocytes causes membrane potential depolarization. Glia, 1, 219-224.