Chloride channelopathies of CLC-2

International Journal of Molecular Sciences

Volumn 15, Issue 1, 2014, Pages 218-249

  Bi, Miao Miao ^a,b   Hong, Sen ^c   Zhou, Hong Yan ^b   Wang, Hong Wei ^d   Wang, Li Na ^b   Zheng, Ya Juan ^a  

^a THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

^b JILIN UNIVERSITY   (China)

^c THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^d QIQIHAR MEDICAL UNIVERSITY   (China)

Author keywords

CLC 2; CLC 2 channels; CLC 2 chloride channelopathies; CLCs

Indexed keywords

5 NITRO 2 (3 PHENYLPROPYLAMINO) BENZOIC ACID; ADENOSINE TRIPHOSPHATE; CASPASE 2; CHLORIDE CHANNEL; CHLORIDE CHANNEL 2; CYCLIC AMP DEPENDENT PROTEIN KINASE; EFENAMIC ACID; EPIDERMAL GROWTH FACTOR RECEPTOR; HEAT SHOCK PROTEIN 70; JANUS KINASE 2; LUBIPROSTONE; OMEPRAZOLE; PILOCARPINE; PLACEBO; STILBENE DERIVATIVE; TAMOXIFEN; TRANSCRIPTION FACTOR SP1; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; CHLORIDE; CLC-2 CHLORIDE CHANNELS;

ACIDIFICATION; CARDIOVASCULAR DISEASE; CELL PROLIFERATION; CELL VOLUME; CHLORIDE CHANNELOPATHY; CONSTIPATION; EYE DISEASE; GENETIC TRANSCRIPTION; HORMONAL REGULATION; HUMAN; IRRITABLE COLON; MALE INFERTILITY; MEMBRANE STEADY POTENTIAL; NERVE CELL EXCITABILITY; NEUROLOGIC DISEASE; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; STRUCTURE ACTIVITY RELATION; TIGHT JUNCTION; UBIQUITINATION; ANIMAL; CHANNELOPATHY; CHEMISTRY; GENETICS; HEART MUSCLE CELL; METABOLISM; PATHOPHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

MAMMALIA; NEMATODA;

ANIMALS; CHANNELOPATHIES; CHLORIDE CHANNELS; CHLORIDES; HUMANS; MYOCYTES, CARDIAC; PROMOTER REGIONS, GENETIC; PROTEIN STRUCTURE, TERTIARY;

EID: 84891476684     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15010218     Document Type: Review

References (146)

1. Dutzler, R. The ClC family of chloride channels and transporters. Curr. Opin. Struct. Biol. 2006, 16, 439-446.
2. Jentsch, T.J. CLC chloride channels and transporters: From genes to protein structure, pathology and physiology. Crit. Rev. Biochem. Mol. Biol. 2008, 43, 3-36.
3. Zifarelli, G.; Pusch, M. CLC Chloride channels and transporters: A biophysical and physiological perspective. Rev. Physiol. Biochem. Pharmacol. 2007, 158, 23-76.
4. Duran, C.; Thompson, C.H.; Xiao, Q.; Hartzell, C. Chloride channels: Often enigmatic, rarely predictable. Annu. Rev. Physiol. 2010, 72, 95-121.
5. Gründer, S.; Thiemann, A.; Pusch, M.; Jentsch, T.J. Regions involved in the opening of CIC-2 chloride channel by voltage and cell volume. Nature 1992, 360, 759-762.
6. Furukawa, T.; Ogura, T.; Katayama, Y.; Hiraoka, M. Characteristics of rabbit ClC-2 current expressed in Xenopus oocytes and its contribution to volume regulation. Am. J. Physiol.-Cell Physiol. 1998, 274, C500-C512.
7. Middleton, R.E.; Pheasant, D.J.; Miller, C. Homodimeric architecture of a ClC-type chloride ion channel. Nature 1996, 383, 337-340.
8. Hsiao, S.H.; Parrish, A.R.; Nahm, S.S.; Abbott, L.C.; McCool, B.A.; Frye, G.D. Effects of early postnatal ethanol intubation on GABAergic synaptic proteins. Dev. Brain Res. 2002, 138, 177-185.
9. Zuniga, L.; Niemeyer, M.I.; Varela, D.; Catalan, M.; Cid, L.P.; Sepulveda, F.V. The voltage-dependent ClC-2 chloride channel has a dual gating mechanism. J. Physiol. 2004, 555, 671-682.
10. Cid, L.P.; Montrose-Rafizadeh, C.; Smith, D.I.; Guggino, W.B.; Cutting, G.R. Cloning of a putative human voltage-gated chloride channel (CIC-2) cDNA widely expressed in human tissues. Hum. Mol. Genet. 1995, 4, 407-413.
11. Planells-Cases, R.; Jentsch, T.J. Chloride channelopathies. Biochim. Biophys. Acta 2009, 1792, 173-189.
12. Hartzell, C.; Qu, Z.; Putzier, I.; Artinian, L.; Chien, L.-T.; Cui, Y. Looking chloride channels straight in the eye: Bestrophins, lipofuscinosis, and retinal degeneration. Physiology 2005, 20, 292-302.
13. Duan, D. Phenomics of cardiac chloride channels: The systematic study of chloride channel function in the heart. J. Physiol. 2009, 587, 2163-2177.
14. Strange, K. Of mice and worms: Novel insights into ClC-2 anion channel physiology. Physiology 2002, 17, 11-16.
15. Duan, D.; Ye, L.; Britton, F.; Horowitz, B.; Hume, J.R. A novel anionic inward rectifier in native cardiac myocytes. Circ. Res. 2000, 86, e63-e71.
16. Hume, J.R.; Duan, D.; Collier, M.L.; Yamazaki, J.; Horowitz, B. Anion transport in heart. Physiol. Rev. 2000, 80, 31-81.
17. Niemeyer, M.I.; Cid, L.P.; Yusef, Y.R.; Briones, R.; Sepúlveda, F.V. Voltage-dependent and-independent titration of specific residues accounts for complex gating of a ClC chloride channel by extracellular protons. J. Phys. 2009, 587, 1387-1400.
18. Weinreich, F.; Jentsch, T.J. Pores formed by single subunits in mixed dimers of different CLC chloride channels. J. Biol. Chem. 2001, 276, 2347-2353.
19. Stölting, G.; Teodorescu, G.; Begemann, B.; Schubert, J.; Nabbout, R.; Toliat, M.R.; Sander, T.; Nürnberg, P.; Lerche, H.; Fahlke, C. Regulation of ClC-2 gating by intracellular ATP. Pflügers Arch. 2013, 465, 1423-1437.
20. Britton, F.C.; Wang, G.L.; Huang, Z.M.; Ye, L.; Horowitz, B.; Hume, J.R.; Duan, D. Functional characterization of novel alternatively spliced ClC-2 chloride channel variants in the heart. J. Biol. Chem. 2005, 280, 25871-25880.
21. Pusch, M.; Jordt, S.-E.; Stein, V.; Jentsch, T.J. Chloride dependence of hyperpolarization-activated chloride channel gates. J. Physiol. 1999, 515, 341-353.
22. Thiemann, A.; Gründer, S.; Pusch, M.; Jentsch, T.J. A chloride channel widely expressed in epithelial and non-epithelial cells. Nature 1992, 356, 57-60.
23. Thompson, C.H.; Olivetti, P.R.; Fuller, M.D.; Freeman, C.S.; McMaster, D.; French, R.J.; Pohl, J.; Kubanek, J.; McCarty, N.A. Isolation and characterization of a high affinity peptide inhibitor of ClC-2 chloride channels. J. Biol. Chem. 2009, 284, 26051-26062.
24. Cuppoletti, J.; Tewari, K.P.; Sherry, A.M.; Kupert, E.Y.; Malinowska, D.H. ClC-2 Cl& channels in human lung epithelia: Activation by arachidonic acid, amidation, and acid-activated omeprazole. Am. J. Physiol.-Cell Physiol. 2001, 281, C46-C54.
25. Besancon, M.; Simon, A.; Sachs, G.; Shin, J.M. Sites of reaction of the gastric H, K-ATPase with extracytoplasmic thiol reagents. J. Biol. Chem. 1997, 272, 22438-22446.
26. Keeling, D.J.; Fallowfield, C.; Milliner, K.J.; Tingley, S.K.; Ife, R.J.; Underwood, A.H. Studies on the mechanism of action of omeprazole. Biochem. Pharmacol. 1985, 34, 2967-2973.
27. Crowell, M.D.; Harris, L.A.; DiBaise, J.K.; Olden, K.W. Activation of type-2 chloride channels: A novel therapeutic target for the treatment of chronic constipation. Curr. Opin. Invest. Drugs 2007, 8, 66-70.
28. Lacy, B.E.; Chey, W.D. Lubiprostone: Chronic constipation and irritable bowel syndrome with constipation. 2009, 10, 143-152.
29. Rivkin, A.; Chagan, L. Lubiprostone: Chloride channel activator for chronic constipation. Clin. Ther. 2006, 28, 2008-2021.
30. Ludewig, U.; Pusch, M.; Jentsch, T.J. Two physically distinct pores in the dimeric ClC-0 chloride channel. Nature 1996, 383, 340-343.
31. Dutzler, R.; Campbell, E.B.; Cadene, M.; Chait, B.T.; MacKinnon, R. X-ray structure of a ClC chloride channel at 3.0 A reveals the molecular basis of anion selectivity. Nature 2002, 415, 287-294.
32. Niemeyer, M.I.; Cid, L.P.; Zúñiga, L.; Catalán, M.; Sepúlveda, F.V. A conserved pore-lining glutamate as a voltage-and chloride-dependent gate in the ClC-2 chloride channel. J. Physiol. 2003, 553, 873-879.
33. Jordt, S.-E.; Jentsch, T.J. Molecular dissection of gating in the ClC-2 chloride channel. EMBO J. 1997, 16, 1582-1592.
34. Varela, D.; Niemeyer, M.I.; Cid, L.P.; Sepúlveda, F.V. Effect of an N-terminus deletion on voltage-dependent gating of the ClC-2 chloride channel. J. Physiol. 2002, 544, 363-372.
35. Haug, K.; Warnstedt, M.; Alekov, A.K.; Sander, T.; Ramírez, A.; Poser, B.; Maljevic, S.; Hebeisen, S.; Kubisch, C.; Rebstock, J. Mutations in CLCN2 encoding a voltage-gated chloride channel are associated with idiopathic generalized epilepsies. Nat. Genet. 2003, 33, 527-532.
36. Garcia-Olivares, J.; Alekov, A.; Boroumand, M.R.; Begemann, B.; Hidalgo, P.; Fahlke, C. Gating of human ClC-2 chloride channels and regulation by carboxy-terminal domains. J. Physiol. 2008, 586, 5325-5336.
37. Stroffekova, K.; Kupert, E.Y.; Malinowska, D.H.; Cuppoletti, J. Identification of the pH sensor and activation by chemical modification of the ClC-2G Cl& channel. Am. J. Physiol.-Cell Physiol. 1998, 275, C1113-C1123.
38. Chu, S.; Blaisdell, C.J.; Liu, M.-Z.M.; Zeitlin, P.L. Perinatal regulation of the ClC-2 chloride channel in lung is mediated by Sp1 and Sp3. Am. J. Physiol.-Lung Cell. Mol. Physiol. 1999, 276, L614-L624.
39. Bösl, M.R.; Stein, V.; Hübner, C.; Zdebik, A.A.; Jordt, S.-E.; Mukhopadhyay, A.K.; Davidoff, M.S.; Holstein, A.-F.; Jentsch, T.J. Male germ cells and photoreceptors, both dependent on close cell-cell interactions, degenerate upon ClC-2 Cl& channel disruption. EMBO J. 2001, 20, 1289-1299.
40. Gong, Y.; Slee, R.B.; Fukai, N.; Rawadi, G.; Roman-Roman, S.; Reginato, A.M.; Wang, H.; Cundy, T.; Glorieux, F.H.; Lev, D. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 2001, 107, 513-523.
41. Duan, D.; Hume, J.R.; Nattel, S. Evidence that outwardly rectifying Cl& channels underlie volume-regulated Cl& currents in heart. Circ. Res. 1997, 80, 103-113.
42. Nehrke, K.; Arreola, J.; Nguyen, H.-V.; Pilato, J.; Richardson, L.; Okunade, G.; Baggs, R.; Shull, G.E.; Melvin, J.E. Loss of hyperpolarization-activated Cl& current in salivary acinar cells from Clcn2 knockout mice. J. Biol. Chem. 2002, 277, 23604-23611.
43. Moeser, A.J.; Haskell, M.M.; Shifflett, D.E.; Little, D.; Schultz, B.D.; Blikslager, A.T. ClC-2 chloride secretion mediates prostaglandin-induced recovery of barrier function in ischemia-injured porcine ileum. Gastroenterology 2004, 127, 802-815.
44. Moeser, A.J.; Nighot, P.K.; Engelke, K.J.; Ueno, R.; Blikslager, A.T. Recovery of mucosal barrier function in ischemic porcine ileum and colon is stimulated by a novel agonist of the ClC-2 chloride channel, lubiprostone. Am. J. Physiol.-Gastrointest. Liver Physiol. 2007, 292, G647-G656.
45. Nighot, P.K.; Moeser, A.J.; Ryan, K.A.; Ghashghaei, T.; Blikslager, A.T. ClC-2 is required for rapid restoration of epithelial tight junctions in ischemic-injured murine jejunum. Exp. Cell Res. 2009, 315, 110-118.
46. Turner, J.R. Molecular basis of epithelial barrier regulation: From basic mechanisms to clinical application. Am. J. Pathol. 2006, 169, 1901-1909.
47. Nighot, P.K.; Blikslager, A.T. ClC-2 regulates mucosal barrier function associated with structural changes to the villus and epithelial tight junction. Am. J. Physiol.-Gastrointest. Liver Physiol. 2010, 299, G449-G456.
48. Nighot, P.K.; Blikslager, A.T. Chloride channel ClC-2 modulates tight junction barrier function via intracellular trafficking of occludin. Am. J. Physiol.-Cell Physiol. 2012, 302, C178-C187.
49. Boyett, M.R.; Honjo, H.; Kodama, I. The sinoatrial node, a heterogeneous pacemaker structure. Cardiovasc. Res. 2000, 47, 658-687.
50. Dobrev, D. Ion channel portrait of the human sinus node: Useful for a better understanding of sinus node function and dysfunction in humans? Circulation 2009, 119, 1556-1558.
51. Chandler, N.J.; Greener, I.D.; Tellez, J.O.; Inada, S.; Musa, H.; Molenaar, P.; Difrancesco, D.; Baruscotti, M.; Longhi, R.; Anderson, R.H.; et al. Molecular architecture of the human sinus node: Insights into the function of the cardiac pacemaker. Circulation 2009, 119, 1562-1575.
52. Verkerk, A.O.; van Ginneken, A.C.; Wilders, R. Pacemaker activity of the human sinoatrial node: Role of the hyperpolarization-activated current, I(f). Int. J. Cardiol. 2009, 132, 318-336.
53. Monfredi, O.; Dobrzynski, H.; Mondal, T.; Boyett, M.R.; Morris, G.M. The anatomy and physiology of the sinoatrial node--a contemporary review. Pacing Clin. Electrophysiol. 2010, 33, 1392-1406.
54. Huang, Z.M.; Prasad, C.; Britton, F.C.; Ye, L.L.; Hatton, W.J.; Duan, D. Functional role of CLC-2 chloride inward rectifier channels in cardiac sinoatrial nodal pacemaker cells. J. Mol. Cell. Cardiol. 2009, 47, 121-132.
55. Enz, R.; Ross, B.J.; Cutting, G.R. Expression of the voltage-gated chloride channel ClC-2 in rod bipolar cells of the rat retina. J. Neurosci. 1999, 19, 9841-9847.
56. Bayes-Genis, A.; Conover, C.A.; Schwartz, R.S. The insulin-like growth factor axis a review of atherosclerosis and restenosis. Circ. Res. 2000, 86, 125-130.
57. Delafontaine, P. Insulin-like growth factor I and its binding proteins in the cardiovascular system. Cardiovasc. Res. 1995, 30, 825-834.
58. Cheng, G.; Kim, M.-J.; Jia, G.; Agrawal, D.K. Involvement of chloride channels in IGF-I-induced proliferation of porcine arterial smooth muscle cells. Cardiovasc. Res. 2007, 73, 198-207.
59. Yang, X.; Lai, X.; Zhang, Y.; Pei, J.; Yang, A.; Zhou, S. Sirna-mediated silencing of ClC-2 gene inhibits proliferation of human U-87 glioma cells. Ai Zheng 2006, 25, 805-810 (in Chinese).
60. Staley, K. The role of an inwardly rectifying chloride conductance in postsynaptic inhibition. J. Neurophysiol. 1994, 72, 273-284.
61. Smith, R.; Clayton, G.; Wilcox, C.; Escudero, K.; Staley, K. Differential expression of an inwardly rectifying chloride conductance in rat brain neurons: A potential mechanism for cell-specific modulation of postsynaptic inhibition. J. Neurosci. 1995, 15, 4057-4067.
62. Staley, K.; Smith, R.; Schaack, J.; Wilcox, C.; Jentsch, T.J. Alteration of GABAA receptor function following gene transfer of the CLC-2 chloride channel. Neuron 1996, 17, 543-551.
63. Rinke, I.; Artmann, J.; Stein, V. ClC-2 voltage-gated channels constitute part of the background conductance and assist chloride extrusion. J. Neurosci. 2010, 30, 4776-4786.
64. Foldy, C.; Lee, S.H.; Morgan, R.J.; Soltesz, I. Regulation of fast-spiking basket cell synapses by the chloride channel ClC-2. Nat. Neurosci. 2010, 13, 1047-1049.
65. Ratté, S.; Prescott, S.A. ClC-2 channels regulate neuronal excitability, not intracellular chloride levels. J. Neurosci. 2011, 31, 15838-15843.
66. Murray, C.B.; Morales, M.M.; Flotte, T.R.; McGrath-Morrow, S.A.; Guggino, W.B.; Zeitlin, P.L. CIC-2: A developmentally dependent chloride channel expressed in the fetal lung and downregulated after birth. Am. J. Respir. Cell Mol. Biol. 1995, 12, 597-604.
67. Schwiebert, E.M.; Cid-Soto, L.P.; Stafford, D.; Carter, M.; Blaisdell, C.J.; Zeitlin, P.L.; Guggino, W.B.; Cutting, G.R. Analysis of ClC-2 channels as an alternative pathway for chloride conduction in cystic fibrosis airway cells. Proc. Natl. Acad. Sci. USA 1998, 95, 3879-3884.
68. Huber, S.; Schröppel, B.; Kretzler, M.; Schlöndorff, D.; Horster, M. Single cell RT-PCR analysis of ClC-2 mRNA expression in ureteric bud tip. Am. J. Physiol.-Renal Physiol. 1998, 274, F951-F957.
69. Malinowska, D.H.; Kupert, E.Y.; Bahinski, A.; Sherry, A.; Cuppoletti, J. Cloning, functional expression, and characterization of a PKA-activated gastric Cl-channel. Am. J. Physiol.-Cell Physiol. 1995, 268, C191-C200.
70. Sander, T.; Schulz, H.; Saar, K.; Gennaro, E.; Riggio, M.C.; Bianchi, A.; Zara, F.; Luna, D.; Bulteau, C.; Kaminska, A. Genome search for susceptibility loci of common idiopathic generalised epilepsies. Hum. Mol. Genet. 2000, 9, 1465-1472.
71. Protopopov, A.; Gizatullin, R.; Vorobieva, N.; Protopopova, M.; Kiss, C.; Kashuba, V.; Klein, G.; Kisselev, L.; Graphodatsky, A.; Zabarovsky, E. Human chromosome 3: High-resolution fluorescencein situ hybridization mapping of 40 uniqueNotl linking clones homologous to genes and cDNAs. Chromosome Res. 1996, 4, 443-447.
72. Holmes, K.W.; Hales, R.; Chu, S.; Maxwell, M.J.; Mogayzel, P.J., Jr.; Zeitlin, P.L. Modulation of Sp1 and Sp3 in lung epithelial cells regulates ClC-2 chloride channel expression. Am. J. Respirat. Cell Mol. Biol. 2003, 29, 499-505.
73. Vij, N.; Zeitlin, P.L. Regulation of the ClC-2 lung epithelial chloride channel by glycosylation of SP1. Am. J. Respirat. Cell Mol. Biol. 2006, 34, 754.
74. Palmada, M.; Dieter, M.; Boehmer, C.; Waldegger, S.; Lang, F. Serum and glucocorticoid inducible kinases functionally regulate ClC-2 channels. Biochem. Biophys. Res. Commun. 2004, 321, 1001-1006.
75. Blaisdell, C.J.; Pellettieri, J.P.; Loughlin, C.E.; Chu, S.; Zeitlin, P.L. Keratinocyte growth factor stimulates CLC-2 expression in primary fetal rat distal lung epithelial cells. Am. J. Respirat. Cell Mol. Biol. 1999, 20, 842-847.
76. Chu, S.; Blaisdell, C.J.; Bamford, P.; Ferro, T.J. Interferon-γ regulates ClC-2 chloride channel in lung epithelial cells. Biochem. Biophys. Res. Commun. 2004, 324, 31-39.
77. Hicke, L. A new ticket for entry into budding vesicles-ubiquitin. Cell 2001, 106, 527-530.
78. Shen, M.-R.; Droogmans, G.; Eggermont, J.; Voets, T.; Ellory, J.C.; Nilius, B. Differential expression of volume-regulated anion channels during cell cycle progression of human cervical cancer cells. J. Physiol. 2000, 529, 385-394.
79. Voets, T.; Szücs, G.; Droogmans, G.; Nilius, B. Blockers of volume-activated Cl& currents inhibit endothelial cell proliferation. Pflügers Arch. 1995, 431, 132-134.
80. Furukawa, T.; Ogura, T.; Zheng, Y.-J.; Tsuchiya, H.; Nakaya, H.; Katayama, Y.; Inagaki, N. Phosphorylation and functional regulation of CIC-2 chloride channels expressed in Xenopus oocytes by M cyclin-dependent protein kinase. J. Physiol. 2002, 540, 883-893.
81. Dhani, S.U.; Kim Chiaw, P.; Huan, L.-J.; Bear, C.E. ATP depletion inhibits the endocytosis of ClC-2. J. Cell. Physiol. 2008, 214, 273-280.
82. Cornejo, I.; Niemeyer, M.I.; Zúñiga, L.; Yusef, Y.R.; Sepúlveda, F.V.; Cid, L.P. Rapid recycling of ClC-2 chloride channels between plasma membrane and endosomes: Role of a tyrosine endocytosis motif in surface retrieval. J. Cell. Physiol. 2009, 221, 650-657.
83. Hosseinzadeh, Z.; Bhavsar, S.K.; Lang, F. Downregulation of ClC-2 by JAK2. Cell. Physiol. Biochem. 2012, 29, 737-742.
84. Ornellas, D.S.; Grozovsky, R.; Goldenberg, R.; Carvalho, D.; Fong, P.; Guggino, W.; Morales, M. Thyroid hormone modulates ClC-2 chloride channel gene expression in rat renal proximal tubules. J. Endocrinol. 2003, 178, 503-511.
85. Ornellas, D.S.; Nascimento, D.S.; Christoph, D.H.; Guggino, W.B.; Morales, M.M. Aldosterone and high-NaCl diet modulate ClC-2 chloride channel gene expression in rat kidney. Pflügers Arch. 2002, 444, 193-201.
86. Nascimento, D.S.; Reis, C.U.; Goldenberg, R.C.; Ortiga-Carvalho, T.M.; Pazos-Moura, C.C.; Guggino, S.E.; Guggino, W.B.; Morales, M.M. Estrogen modulates ClC-2 chloride channel gene expression in rat kidney. Pflügers Arch. 2003, 446, 593-599.
87. Baglole, C.J.; Sigalet, D.L.; Meddings, J.B. α1-adrenoceptors down-regulate ClC-2 chloride channels in epithelial cells from the acutely denervated jejunum. Eur. J. Pharmacol. 2007, 565, 202-206.
88. Dhani, S.U.; Mohammad-Panah, R.; Ahmed, N.; Ackerley, C.; Ramjeesingh, M.; Bear, C.E. Evidence for a functional interaction between the ClC-2 chloride channel and the retrograde motor dynein complex. J. Biol. Chem. 2003, 278, 16262-16270.
89. Cuppoletti, J.; Baker, A.; Malinowska, D.H. Cl-channels of the gastric parietal cell that are active at low pH. Am. J. Physiol.-Cell Physiol. 1993, 264, C1609-C1618.
90. Sherry, A.; Stroffekova, K.; Knapp, L.M.; Kupert, E.Y.; Cuppoletti, J.; Malinowska, D. Characterization of the human pH-and PKA-activated ClC-2G (2 alpha) Cl-channel. Am. J. Physiol.-Cell Physiol. 1997, 273, C384-C393.
91. Tewari, K.P.; Malinowska, D.H.; Sherry, A.M.; Cuppoletti, J. PKA and arachidonic acid activation of human recombinant ClC-2 chloride channels. Am. J. Physiol.-Cell Physiol. 2000, 279, C40-C50.
92. Klaus, F.; Laufer, J.; Czarkowski, K.; Strutz-Seebohm, N.; Seebohm, G.; Lang, F. PIKfyve-dependent regulation of the Cl& channel ClC-2. Biochem. Biophys. Res. Commun. 2009, 381, 407-411.
93. Duan, D.; Ye, L.; Britton, F.; Miller, L.J.; Yamazaki, J.; Horowitz, B.; Hume, J.R. Purinoceptor-coupled Cl& channels in mouse heart: A novel, alternative pathway for CFTR regulation. J. Physiol. 1999, 521, 43-56.
94. Nagasaki, M.; Ye, L.; Duan, D.; Horowitz, B.; Hume, J.R. Intracellular cyclic AMP inhibits native and recombinant volume-regulated chloride channels from mammalian heart. J. Physiol. 2000, 523, 705-717.
95. Kajita, H.; Omori, K.; Matsuda, H. The chloride channel ClC-2 contributes to the inwardly rectifying Cl& conductance in cultured porcine choroid plexus epithelial cells. J. Physiol. 2000, 523, 313-324.
96. Cuppoletti, J.; Tewari, K.P.; Sherry, A.M.; Ferrante, C.J.; Malinowska, D.H. Sites of protein kinase A activation of the human ClC-2 Cl-channel. J. Biol. Chem. 2004, 279, 21849-21856.
97. Charles-Schoeman, C.; Watanabe, J.; Lee, Y.Y.; Furst, D.E.; Amjadi, S.; Elashoff, D.; Park, G.; McMahon, M.; Paulus, H.E.; Fogelman, A.M. Abnormal function of high-density lipoprotein is associated with poor disease control and an altered protein cargo in rheumatoid arthritis. Arthritis Rheum. 2009, 60, 2870-2879.
98. Sorota, S. Tyrosine protein kinase inhibitors prevent activation of cardiac swelling-induced chloride current. Pflügers Arch. 1995, 431, 178-185.
99. Tilly, B.; van den Berghe, N.; Tertoolen, L.; Edixhoven, M.J.; de Jonge, H.R. Protein tyrosine phosphorylation is involved in osmoregulation of ionic conductances. J. Biol. Chem. 1993, 268, 19919-19922.
100. Voets, T.; Manolopoulos, V.; Eggermont, J.; Ellory, C.; Droogmans, G.; Nilius, B. Regulation of a swelling-activated chloride current in bovine endothelium by protein tyrosine phosphorylation and G proteins. J. Physiol. 1998, 506, 341-352.
101. Bali, M.; Lipecka, J.; Edelman, A.; Fritsch, J. Regulation of ClC-2 chloride channels in T84 cells by TGF-α. Am. J. Physiol.-Cell Physiol. 2001, 280, C1588-C1598.
102. Smith, D.F.; Whitesell, L.; Katsanis, E. Molecular chaperones: Biology and prospects for pharmacological intervention. Pharmacol. Rev. 1998, 50, 493-514.
103. Pratt, W.B. The role of Thehsp90-based chaperone system in signal transduction by nuclear receptors and receptors signaling via map kinase. Annu. Rev. Pharmacol. Toxicol. 1997, 37, 297-326.
104. Hinzpeter, A.; Lipecka, J.; Brouillard, F.; Baudoin-Legros, M.; Dadlez, M.; Edelman, A.; Fritsch, J. Association between Hsp90 and the ClC-2 chloride channel upregulates channel function. Am. J. Physiol.-Cell Physiol. 2006, 290, C45-C56.
105. Ahmed, N.; Ramjeesingh, M.; Wong, S.; Varga, A.; Garami, E.; Bear, C. Chloride channel activity of ClC-2 is modified by the actin cytoskeleton. Biochem. J. 2000, 352, 789-794.
106. Hinzpeter, A.; Fritsch, J.; Borot, F.; Trudel, S.; Vieu, D.-L.; Brouillard, F.; Baudouin-Legros, M.; Clain, J.; Edelman, A.; Ollero, M. Membrane cholesterol content modulates ClC-2 gating and sensitivity to oxidative stress. J. Biol. Chem. 2007, 282, 2423-2432.
107. Zeuthen, T.; Hamann, S.; La Cour, M. Cotransport of H+, lactate and H2O by membrane proteins in retinal pigment epithelium of bullfrog. J. Physiol. 1996, 497, 3-17.
108. Philp, N.J.; Yoon, H.; Grollman, E.F. Monocarboxylate transporter MCT1 is located in the apical membrane and MCT3 in the basal membrane of rat RPE. Am. J. Physiol.-Regul. Integr. Comp. Physiol. 1998, 274, R1824-R1828.
109. Edwards, M.M.; de Evsikova, C.M.; Collin, G.B.; Gifford, E.; Wu, J.; Hicks, W.L.; Whiting, C.; Varvel, N.H.; Maphis, N.; Lamb, B.T. Photoreceptor degeneration, azoospermia, leukoencephalopathy, and abnormal RPE cell function in mice expressing an early stop mutation in CLCN2. Invest. Ophthalmol. Visual Sci. 2010, 51, 3264-3272.
110. Pflugfelder, S.C.; Tseng, S.C.; Sanabria, O.; Kell, H.; Garcia, C.G.; Felix, C.; Feuer, W.; Reis, B.L. Evaluation of subjective assessments and objective diagnostic tests for diagnosing tear-film disorders known to cause ocular irritation. Cornea 1998, 17, 38.
111. Nandoskar, P.; Wang, Y.; Wei, R.; Liu, Y.; Zhao, P.; Lu, M.; Huang, J.; Thomas, P.; Trousdale, M.D.; Ding, C. Changes of chloride channels in the lacrimal glands of a rabbit model of Sjögren's Syndrome. Cornea 2012, 31, 273.
112. Gyömörey, K.; Yeger, H.; Ackerley, C.; Garami, E.; Bear, C.E. Expression of the chloride channel ClC-2 in the murine small intestine epithelium. Am. J. Physiol.-Cell Physiol. 2000, 279, C1787-C1794.
113. Murek, M.; Kopic, S.; Geibel, J. Evidence for intestinal chloride secretion. Exp. Physiol. 2010, 95, 471-478.
114. Catalán, M.; Cornejo, I.; Figueroa, C.D.; Niemeyer, M.I.; Sepúlveda, F.V.; Cid, L.P. ClC-2 in guinea pig colon: mRNA, immunolabeling, and functional evidence for surface epithelium localization. Am. J. Physiol.-Gastrointest. Liver Physiol. 2002, 283, G1004-G1013.
115. Lipecka, J.; Bali, M.; Thomas, A.; Fanen, P.; Edelman, A.; Fritsch, J. Distribution of ClC-2 chloride channel in rat and human epithelial tissues. Am. J. Physiol.-Cell Physiol. 2002, 282, C805-C816.
116. Catalán, M.; Niemeyer, M.I.; Cid, L.P.; Sepúlveda, F.V. Basolateral ClC-2 chloride channels in surface colon epithelium: Regulation by a direct effect of intracellular chloride. Gastroenterology 2004, 126, 1104-1114.
117. Catalán, M.A.; Flores, C.A.; González-Begne, M.; Zhang, Y.; Sepúlveda, F.V.; Melvin, J.E. Severe defects in absorptive ion transport in distal colons of mice that lack ClC-2 channels. Gastroenterology 2012, 142, 346-354.
118. Inagaki, A.; Yamaguchi, S.; Takahashi-Iwanaga, H.; Iwanaga, T.; Ishikawa, T. Functional characterization of a ClC-2-like Cl& conductance in surface epithelial cells of rat rectal colon. J. Membr. Biol. 2010, 235, 27-41.
119. Ben-Ari, Y. Excitatory actions of GABA during development: The nature of the nurture. Nat. Rev. Neurosci. 2002, 3, 728-739.
120. Madison, D.V.; Malenka, R.C.; Nicoll, R.A. Phorbol esters block a voltage-sensitive chloride current in hippocampal pyramidal cells. Nature 1986, 321, 695-697.
121. Cossette, P.; Liu, L.; Brisebois, K.; Dong, H.; Lortie, A.; Vanasse, M.; Saint-Hilaire, J.-M.; Carmant, L.; Verner, A.; Lu, W.-Y. Mutation of GABRA1 in an autosomal dominant form of juvenile myoclonic epilepsy. Nat. Genet. 2002, 31, 184-189.
122. Ge, Y.-X.; Liu, Y.; Tang, H.-Y.; Liu, X.-G.; Wang, X. ClC-2 contributes to tonic inhibition mediated by α5 subunit-containing GABAA receptor in experimental temporal lobe epilepsy. Neuroscience 2011, 186, 120-127.
123. D'Agostino, D.; Bertelli, M.; Gallo, S.; Cecchin, S.; Albiero, E.; Garofalo, P.; Gambardella, A.; Hilaire, J.-M.S.; Kwiecinski, H.; Andermann, E. Mutations and polymorphisms of the CLCN2 gene in idiopathic epilepsy. Neurology 2004, 63, 1500-1502.
124. Everett, K.; Chioza, B.; Aicardi, J.; Aschauer, H.; Brouwer, O.; Callenbach, P.; Covanis, A.; Dooley, J.; Dulac, O.; Durner, M. Linkage and mutational analysis of CLCN2 in childhood absence epilepsy. Epilepsy Res. 2007, 75, 145-153.
125. Klassen, T.; Davis, C.; Goldman, A.; Burgess, D.; Chen, T.; Wheeler, D.; McPherson, J.; Bourquin, T.; Lewis, L.; Villasana, D.; et al. Exome sequencing of ion channel genes reveals complex profiles confounding personal risk assessment in epilepsy. Cell 2011, 145, 1036-1048.
126. Stogmann, E.; Lichtner, P.; Baumgartner, C.; Schmied, M.; Hotzy, C.; Asmus, F.; Leutmezer, F.; Bonelli, S.; Assem-Hilger, E.; Vass, K. Mutations in the CLCN2 gene are a rare cause of idiopathic generalized epilepsy syndromes. Neurogenetics 2006, 7, 265-268.
127. Combi, R.; Grioni, D.; Contri, M.; Redaelli, S.; Redaelli, F.; Bassi, M.T.; Barisani, D.; Lavitrano, M.L.; Tredici, G.; Tenchini, M.L. Clinical and genetic familial study of a large cohort of Italian children with idiopathic epilepsy. Brain Res. Bull. 2009, 79, 89-96.
128. Saint-Martin, C.; Gauvain, G.; Teodorescu, G.; Gourfinkel-An, I.; Fedirko, E.; Weber, Y.G.; Maljevic, S.; Ernst, J.P.; Garcia-Olivares, J.; Fahlke, C. Two novel CLCN2 mutations accelerating chloride channel deactivation are associated with idiopathic generalized epilepsy. Hum. Mutat. 2009, 30, 397-405.
129. Niemeyer, M.I.; Yusef, Y.R.; Cornejo, I.; Flores, C.A.; Sepúlveda, F.V.; Cid, L.P. Functional evaluation of human ClC-2 chloride channel mutations associated with idiopathic generalized epilepsies. Physiol. Genomics 2004, 19, 74-83.
130. Haug, K.; Warnstedt, M.; Alekov, A.K.; Sander, T.; Ramírez, A.; Poser, B.; Maljevic, S.; Hebeisen, S.; Kubisch, C.; Rebstock, J. Retraction: Mutations in CLCN2 encoding a voltage-gated chloride channel are associated with idiopathic generalized epilepsies. Nat. Genet. 2009, 41, 1043.
131. Blanz, J.; Schweizer, M.; Auberson, M.; Maier, H.; Muenscher, A.; Hübner, C.A.; Jentsch, T.J. Leukoencephalopathy upon disruption of the chloride channel ClC-2. J. Neurosci. 2007, 27, 6581-6589.
132. Cortez, M.; Li, C.; Whitehead, S.; Dhani, S.; D'Antonio, C.; Huan, L.; Bennett, S.; Snead, O.; Bear, C. Disruption of ClC-2 expression is associated with progressive neurodegeneration in aging mice. Neuroscience 2010, 167, 154-162.
133. Van der Knaap, M.; Barth, P.; Stroink, H.; van Nieuwenhuizen, O.; Arts, W.; Hoogenraad, F.; Valk, J. Leukoencephalopathy with swelling and a discrepantly mild clinical course in eight children. Ann. Neurol. 1995, 37, 324-334.
134. Duarri, A.; Lopez de Heredia, M.; Capdevila-Nortes, X.; Ridder, M.C.; Montolio, M.; López-Hernández, T.; Boor, I.; Lien, C.-F.; Hagemann, T.; Messing, A. Knockdown of MLC1 in primary astrocytes causes cell vacuolation: A MLC disease cell model. Neurobiol. Dis. 2011, 43, 228-238.
135. Brignone, M.S.; Lanciotti, A.; Macioce, P.; Macchia, G.; Gaetani, M.; Aloisi, F.; Petrucci, T.C.; Ambrosini, E. 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. Hum. Mol. Genet. 2011, 20, 90-103.
136. Jeworutzki, E.; López-Hernández, T.; Capdevila-Nortes, X.; Sirisi, S.; Bengtsson, L.; Montolio, M.; Zifarelli, G.; Arnedo, T.; Müller, C.S.; Schulte, U. GlialCAM, a Protein Defective in a Leukodystrophy, Serves as a ClC-2 Cl& Channel Auxiliary Subunit. Neuron 2012, 73, 951-961.
137. Scheper, G.C.; van Berkel, C.G.; Leisle, L.; de Groot, K.E.; Errami, A.; Jentsch, T.J.; van der Knaap, M.S. Analysis of CLCN2 as candidate gene for megalencephalic leukoencephalopathy with subcortical cysts. Genet. Test. Mol. Biomark. 2010, 14, 255-257.
138. Yankaskas, J.R.; Marshall, B.C.; Sufian, B.; Simon, R.H.; Rodman, D. Cystic fibrosis adult careconsensus conference report. CHEST J. 2004, 125, 1S-39S.
139. Cuppoletti, J.; Malinowska, D.H. Ca2+-activated Cl& channels Focus on Molecular cloning and transmembrane structure of hCLCA2 from human lung, trachea, and mammary gland". Am. J. Physiol.-Cell Physiol. 1999, 276, C1259-C1260.
140. Blaisdell, C.J.; Howard, T.D.; Stern, A.; Bamford, P.; Bleecker, E.R.; Stine, O.C. CLC-2 single nucleotide polymorphisms (SNPs) as potential modifiers of cystic fibrosis disease severity. BMC Med. Genet. 2004, 5, 26.
141. Komukai, K.; Brette, F.; Pascarel, C.; Orchard, C.H. Electrophysiological response of rat ventricular myocytes to acidosis. Am. J. Physiol.-Heart Circ. Physiol. 2002, 283, H412-H422.
142. Ackerman, M.J.; Clapham, D.E. Cardiac chloride channels. Trends Cardiovasc. Med. 1993, 3, 23-28.
143. Harvey, R.D. Cardiac chloride currents. Physiology 1996, 11, 175-181.
144. Hiraoka, M.; Kawano, S.; Hirano, Y.; Furukawa, T. Role of cardiac chloride currents in changes in action potential characteristics and arrhythmias. Cardiovasc. Res. 1998, 40, 23-33.
145. Sorota, S. Insights into the structure, distribution and function of the cardiac chloride channels. Cardiovasc. Res. 1999, 42, 361-376.
146. Britton, F.C.; Hatton, W.J.; Rossow, C.F.; Duan, D.; Hume, J.R.; Horowitz, B. Molecular distribution of volume-regulated chloride channels (ClC-2 and ClC-3) in cardiac tissues. Am. J. Physiol. Heart Circ. Physiol. 2000, 279, H2225-H2233.