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Research Article

Challenging accepted ion channel biology: p64 and the CLIC family of putative intracellular anion channel proteins (Review)

Pages 1-11 | Published online: 09 Jul 2009

References

  • Al-Awqati, Q., 1994, An IAA-sensitive vacuolar chloride channel. Current Topics in Membranes, 42, 59 - 72.
  • Al-Awqati, Q., 1995, Chloride channels of intracellular organelles. Current Opinions in Cell Biology, 7, 504 - 508.
  • Al-Awqati, Q., Barasch, J. and Landry, D., 1992, Chloride channels of intracellular organelles and their potential role in cystic fibrosis. Journal of Experimental Biology, 172, 245 - 266.
  • Ashley, R. H., 1989, Activation and conductance properties of ryanodine-sensitive calcium channels from brain microsomal membranes incorporated into planar lipid bilayers. Journal of Membrane Biology, 111, 179 - 189.
  • Bae, H. R. and Verkman, A. S., 1990, Protein kinase A regulates chloride conductance in endocytic vesicles from proximal tubule. Nature, 348, 637 - 639.
  • Bauer, C. K., Steinmeyer, K., Schwarz, J. R. and Jentsch, T. J., 1991, Completely functional double-barreled chloride channel expressed from a single Torpedo cDNA. Proceedings of the National Academy of Sciences, USA, 88, 11052- 11056.
  • Bear, C. E., Li, C. H., Kartner, N., Bridges, R. J., Jensen, T. J., Ramjeesingh, M. and Riordan, J. R., 1992, Purification and functional reconstitution of the cystic fibrosis transmembrane conductance regulator (CFTR). Cell, 68, 809 - 818.
  • Berryman, M. and Bretscher, A., 2000, Identification of a novel member of the chloride intracellular channel gene family, CLIC5, that associates with the actin cytoskeleton of placental microvilli. Molecular Biology of the Cell, 11, 1509- 1521.
  • Biwersi, J. and Verkman, A. S., 1994, Functional CFTR in endosomal compartment of CFTR-expressing fibroblasts and T84 cells. American Journal of Physiology, 266, C149- 56.
  • Board, P. G., Coggan, M., Chelvanayagam, G., Easteal, S., Jermiin, L. S., Schulte, G. K., Danley, D. E., Hoth, L. R., Griffor, M. C., Kamath, A. V., Rosner, M. H., Chrunyk, B. A., Perregaux, D. E., Gabel, C. A., Geoghegan, K. F. and Pandit, J., 2000, Identifica- tion, characterization, and crystal structure of the Omega class glutathione transferases. Journal of Biological Chemistry, 275, 24798- 24806.
  • Chuang, J. Z., Milner, T. A., Zhu, M. and Sung, C. H., 1999, A 29 kDa intracellular chloride channel p64H1 is associated with large dense-core vesicles in rat hippocampal neurons. Journal of Neuroscience, 19, 2919- 2928.
  • Clark, A. G., Murray, D. and Ashley, R. H., 1997, Single-channel properties of a rat brain endoplasmic reticulum anion channel. Biophysical Journal, 73, 168 - 178.
  • Colquhoun, D. and Sigworth, F. J., 1983, Fitting and statistical analysis of single channel records. In B. Sakmann and E. Neher (eds), Single Channel Recording (New York: Plenum), pp. 191 - 263.
  • Del Camino, D., Holmgren, M., Liu, Y. and Yellen, G., 2000, Blocker protection in the pore of a voltage-gated K+ channel and its structural implications. Nature, 403, 321 - 325.
  • Doyle, D. A., Cabral, J. M., Pfuetzner, R. A., Kuo, A. L., Gulbis, J. M., Cohen, S. L., Chait, B. T. and Mackinnon, R., 1998, The structure of the potassium channel: Molecular basis of K+ conduction and selectivity. Science, 280, 69 - 77.
  • Dulhunty, A., Gage, P., Curtis, S., Chelvanayagam, G. and Board, P., 2001, The glutathione transferase structural family includes a nuclear chloride channel and a ryanodine receptor calcium release channel modulator. Journal of Biological Chemistry, 276, 3319- 3323.
  • Duncan, R. R., Westwood, P. K., Boyd, A. and Ashley, R. H., 1997, Rat brain p64H1, expression of a new member of the p64 chloride channel protein family in endoplasmic reticulum. Journal of Biological Chemistry, 272, 23880- 23886.
  • Dutzler, R., Campbell, E. B., Cadene, M., Chait, B. T. and Mackinnon, R., 2002, X-ray structure of a ClC chloride channel at 3. 0 A0 reveals the molecular basis of anion selectivity. Nature, 415, 287 - 294.
  • Edwards, J. C., 1999, A novel p64-related Cl- channel: subcellular distribution and nephron segment-specific expression. American Journal of Physiology, 276, F398 - F408.
  • Edwards, J. C. and Kapadia, S., 2000, Regulation of the bovine kidney microsomal chloride channel p64 by p59fyn, a Src family tyrosine kinase. Journal of Biological Chemistry, 275, 31826- 31832.
  • Edwards, J. C., Tulk, B. and Schlesinger, P. H., 1998, Functional expression of p64, an intracellular chloride channel protein. Journal of Membrane Biology, 163, 119 - 127.
  • Eggermont, J., Trouet, D., Carton, I. and Nilius, B., 2001, Cellular function and control of volume-regulated anion channels. Cell Biochemistry and Biophysics, 35, 263 - 274.
  • Estevez, R., Boettger, T., Stein, V., Birkenhager, R., Otto, E., Hildebrandt, F. and Jentsch, T. J., 2001, Barttin is a Cl- channel beta-subunit crucial for renal Cl- reabsorption and inner ear K+ secretion. Nature, 414, 558 - 561.
  • Fernandez-Salas, E., Sagar, M., Cheng, C., Yuspa, S. H. and Weinberg, W. C., 1999, p53 and tumor necrosis factor alpha regulate the expression of a mitochondrial chloride channel protein. Journal of Biological Chemistry, 274, 36488- 36497.
  • Fernandez-Salas, E., Suh, K. S., Speransky, V. V., Bowers, W. L., Levy, J. M., Adams, T., Pathak, K. R., Edwards, L. E., Hayes, D.D., Cheng, C., Steven, A. C., Weinberg, W. C. and Yuspa, S. H., 2002, mtCLIC/CLIC4, an organellular chloride channel protein, is increased by DNA damage and participates in the apoptotic response to p53. Molecular and Cellular Biology, 22, 3610 - 3620. Frillingos, S., Sahin-Toth, M., Wu, J. and Kaback, H. R., 1998, Cys- scanning mutagenesis: a novel approach to structure function relationships in polytopic membrane proteins. FASEB Journal, 12,1281 - 1299.
  • Gunther, W., Luchow, A., Cluzeaud, F., Vandewalle, A. and Jentsch,T. J., 1998, ClC-5, the chloride channel mutated in Dent’s disease, colocalizes with the proton pump in endocytotically active kidney cells. Proceedings of the National Academy of Sciences, USA, 95, 8075- 8080.
  • Harrop, S. J., DeMaere, M. Z., Fairlie, W. D., Reztsova, T., Valenzuela, S. M., Mazzanti, M., Tonini, R., Qiu, M. R., Jankova, L., Warton, K., Bauskin, A. R., Wu, W. M., Pankhurst, S., Campbell, T. J., Breit, S. N. and Curmi, P. M., 2001, Crystal structure of a soluble form of the intracellular chloride ion channel CLIC1, NCC27, at 1.4-A0 resolution. Journal of BiologicalChemistry, 276, 44993 - 45000.
  • Hayman, K. A. and Ashley, R. H., 1993, Structural features of a multisubstate cardiac mitoplast anion channel: inferences from single-channel recording. Journal of Membrane Biology, 136, 191 - 197.
  • Hayman, K. A., Spurway, T. S. and Ashley, R. H., 1993, Single anion channels reconstituted from cardiac mitoplasts. Journal of Membrane Biology, 136, 181 - 190.
  • Heiss, N. S. and Poustka, A., 1997, Genomic structure of a novel chloride channel gene, CLiC2, in Xq28. Genomics 45, 224 - 228. Hevers, W. and Luddens, H., 1998, The diversity of GABAA receptors. Pharmacological and electrophysiological properties of GABAA channel subtypes. Molecular Neurobiology, 18, 35 - 86. Howell, S., Duncan, R. R. and Ashley, R. H., 1996, Identification and characterisation of a homologue of p64 in rat tissues. FEBS Letters, 390, 207 - 210.
  • Jentsch, T. J., Stein, V., Weinreich, F. and Zdebik, A. A., 2002, Molecular structure and physiological function of chloride chan- nels. Physiological Reviews, 82, 503 - 568.
  • Jentsch, T. J., Steinmeyer, K. and Schwarz, G., 1990, Primary structure of Torpedo marmorata chloride channel isolated by expression cloning in Xenopus oocytes. Nature, 348, 510 - 514.
  • Klughammer, B., Benz, R., Betz, M., Thume, M. and Dietz, K. J., 1992, Reconstitution of vacuolar ion channels into planar lipid bilayers. Biochimica et Biophysica Acta, 1104, 308 - 316.
  • Koch, M. C., Steinmeyer, K., Lorenz, C., Ricker, K., Wolf, F., Otto, M., Zoll, B., Lehmann-Horn, F., Grzeschik, K. H. and Jentsch, T. J., 1992, The skeletal muscle chloride channel in dominant and recessive human myotonia. Science, 257, 797 - 800.
  • Kourie, J. I., Laver, D. R., Junankar, P. R., Gage, P. W. and Dulhunty, A. F., 1996, Characteristics of two types of chloride channel in sarcoplasmic reticulum vesicles from rabbit skeletal muscle. Biophysical Journal, 70, 202 - 221.
  • Landry, D., Sullivan, S., Nicolaides, M., Redhead, C., Edelman, A., Field, M., Al-Awqati, Q. and Edwards, J., 1993, Molecular cloning and characterization of p64, a chloride channel protein from kidney microsomes. Journal of Biological Chemistry, 268, 14948- 14955.
  • Landry, D. W., Akabas, M. A., Redhead, C. and Al-Awqati, Q., 1990, Purification and reconstitution of epithelial chloride channels. Methods in Enzymology, 191, 572 - 582.
  • Landry, D. W., Akabas, M. H., Redhead, C., Edelman, A., Cragoe, E.J. and Al-Awqati, Q., 1989, Purification and reconstitution of chloride channels from kidney and trachea. Science, 244, 1469- 1472.
  • Landry, D. W., Reitman, M., Cragoe, E. R. and Al-Awqati, Q., 1987, Epithelial chloride channels: development of inhibitory ligands. Journal of General Physiology, 90, 779 - 798.
  • Langosch, D., Becker, C. M. and Betz, H., 1990, The inhibitory glycine receptor: a ligand-gated chloride channel of the central nervous system. European Journal of Biochemistry, 194, 1 - 8.
  • Laver, D. R., Lenz, G. K. and Dulhunty, A. F., 2001, Phosphate ion channels in sarcoplasmic reticulum of rabbit skeletal muscle. Journal of Physiology, 535, 715 - 728.
  • Mikoshiba, K., 1997, The InsP3 receptor and intracellular Ca2+ signaling. Current Opinions in Neurobiology, 7, 339 - 345.
  • Miller, C., 1982, Open-state substructure of single chloride channels from Torpedo electroplax. Philosophical Transactions of the Royal Society of London B, 299, 401 - 411.
  • Moorman, J. R., Palmer, C. J., John, J. E., Durieux, M. E. and Jones, L. R., 1992, Phospholemman expression induces a hyperpolar- ization-activated chloride current in Xenopus oocytes. Journal of Biological Chemistry, 267, 14551- 14554.
  • Morier, N. and Sauve·, R., 1994, Analysis of a novel double-barreled anion channel from rat liver rough endoplasmic reticulum. Biophysical Journal, 67, 590 - 602.
  • Morrison, B. W., Moorman, J. R., Kowdley, G. C., Kobayashi, Y. M., Jones, L. R. and Leder, P., 1995, Mat-8, a novel phospholemman- like protein expressed in human breast-tumors, induces a chloride conductance in Xenopus oocytes. Journal of Biological Chemistry, 270, 2176- 2182.
  • Mulberg, A. E., Tulk, B. M. and Forgac, M., 1995, Modulation of coated vesicle chloride channel activity and acidification by reversible protein kinase A-dependent phosphorylation. Journal of Biological Chemistry, 266, 20590- 20593.
  • Nishizawa, T., Nagao, T., Iwatsubo, T., Forte, J. G. and Urushidani, T., 2000, Molecular cloning and characterization of a novel chloride intracellular channel-related protein, parchorin, expressed in water-secreting cells. Journal of Biological Chemistry, 275, 11164- 11173.
  • Nordeen, M. H., Jones, S. M., Howell, K. E. and Caldwell, J. H., 2000, GOLAC: an endogenous anion channel of the Golgi complex. Biophysical Journal, 78, 2918- 2928.
  • Parker, M. W. and Pattus, F., 1993, Rendering a membrane protein soluble in water: a common packing motif in bacterial protein toxins. Trends in Biochemical Sciences, 18, 391 - 395.
  • 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. Clinical and Experimental Pharmacology and Physiology, 27, 901 - 905.
  • Paulmichl, M., Li, Y., Wickman, K., Ackerman, M., Peralta, E. and Clapham, D., 1992, New mammalian chloride channel identified by expression cloning. Nature, 356, 238 - 241.
  • Prat, A. G. and Cantiello, H. F., 1996, Nuclear ion channel activity is regulated by actin filaments. American Journal of Physiology, 270, C1532- 1543.
  • Proutski, I, Karoulias, N, and Ashley, R. H., 2002, Over-expressed Chloride Intracellular Channel protein CLIC4 (p64H1) is an essential component of novel plasma membrane anion channels. Biochemical and Biophysical Research Communications, 297, 317 - 322.
  • Qian, Z., Okuhara, D., Abe, M. K. and Rosner, M. R., 1999, Molecular cloning and characterization of a mitogen-activated protein kinase-associated intracellular chloride channel. Journal of Biological Chemistry, 274, 1621- 1627.
  • Ramjeesingh, M., Li, C., Kogan, I., Wang, Y., Huan, L. J. and Bear, C. E., 2001, A monomer is the minimum functional unit required for channel and ATPase activity of the cystic fibrosis transmem- brane conductance regulator. Biochemistry, 40, 10700- 10706.
  • Ran, S., Fuller, C. M., Arrate, M. P., Latorre, R. and Benos, D. J., 1992, Functional reconstitution of a chloride channel protein from bovine trachea. Journal of Biological Chemistry, 267, 20630- 20637.
  • Redhead, C., Sullivan, S. K., Koseki, C., Fujiwara, K. and Edwards,J. C., 1997, Subcellular distribution and targeting of the intracellular chloride channel p64. Molecular Biology of the Cell, 8, 691 - 704.
  • Redhead, C. R., Edelman, A. E., Brown, D., Landry, D. W. and Al- Awqati, Q., 1992, A ubiquitous 64-kDa protein is a component of a chloride channel of plasma and intracellular membranes. Pro- ceedings of the National Academy of Sciences, USA, 89, 3716- 3720.
  • Reenstra, W. W., Sabolic, I., Bae, H. R. and Verkman, A. S., 1992, Protein kinase A dependent membrane protein phosphorylation and chloride conductance in endosomal vesicles from kidney cortex. Biochemistry, 31, 175 - 181.
  • Riordan, J. R., Rommens, J. M., Kerem, B., Alon, N., Rozmahel, R., Grzelczak, Z., Zielenski, J., Lok, S., Plavsic, N., Chou, J. L., Drumm, M. L., Ianuzzi, M. C., Collins, F. S. and Tsui, L.-C., 1989, Identification of the cystic fibrosis gene: cloning and characteriza- tion of complementary DNA. Science, 245, 1066- 1073.
  • Rosenberg, R. L. and East, J. E., 1992, Cell-free expression of functional Shaker potassium channels. Nature, 360, 166 - 169.
  • Rybak, S. L., Lanni, F. and Murphy, R. F., 1997, Theoretical considerations on the role of membrane potential in the regulation of endosomal pH. Biophysical Journal, 73, 674 - 687.
  • Schein, S. J., Colombini, M. and Finkelstein, A., 1976, Reconstitution in planar lipid bilayers of a voltage-dependent anion-selective channel obtained from Paramecium mitochondria. Journal of Membrane Biology, 30, 99 - 120.
  • Schlesinger, P. H., Blair, H. C., Teitelbaum, S. L. and Edwards, J. C., 1997, Characterization of the osteoclast ruffled border chloride channel and its role in bone resorption. Journal of Biological Chemistry, 272, 18636- 18643.
  • Sheppard, D. N. and Welsh, M. J., 1999, Structure and function of the CFTR chloride channel. Physiological Reviews, 79, S23 - S45. Shoshan-Barmatz, V. and Ashley, R. H., 1998, The structure, function, and cellular regulation of ryanodine-sensitive Ca2+ release channels. international Reviews in Cytology, 183, 185 -270.
  • Simon, S. M. and Blobel, G., 1991, A protein-conducting channel in the endoplasmic reticulum. Cell, 65, 371 - 380.
  • Smith, J. S., Coronado, R. and Meissner, G., 1985, Sarcoplasmic reticulum contains adenine nucleotide-activated calcium channels. Nature, 316, 446 - 449.
  • Stanley, E. F., Ehrenstein, G. and Russell, J. T., 1988, Evidence for anion channels in secretory vesicles. Neuroscience, 25, 1035- 1039.
  • Stobrawa, S. M., Breiderhoff, T., Takamori, S., Engel, D., Schweizer, M., Zdebik, A. A., Bosl, M. R., Ruether, K., Jahn, H., Draguhn, A., Jahn, R. and Jentsch, T. J., 2001, Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron, 29, 185 - 196.
  • Suginta, W., Karoulias, N., Aitken, A. and Ashley, R. H., 2001, Chloride intracellular channel protein CLIC4 (p64H1) binds directly to brain dynamin I in a complex containing actin, tubulin and 14-3- 3 isoforms. Biochemical Journal, 359, 55 - 64.
  • Sukhareva, M., Morrissette, J. and Coronado, R., 1994, Mechanism of chloride-dependent release of Ca2+ in the sarcoplasmic reticulum of rabbit skeletal muscle. Biophysical Journal, 67, 751 - 765.
  • Tabares, L., Mazzanti, M. and Clapham, D. E., 1991, Chloride channels in the nuclear envelope. Journal of Membrane Biology, 123, 49 - 54.
  • Tamir, H., Piscopo, I., Liu, K. P., Hsiung, S. C., Adlersberg, M., Nicolaides, M., AlAwqati, Q., Nunez, E. A. and Gershon, M. D., 1994, Secretagogue-induced gating of chloride channels in the secretory vesicles of parafollicular cells. Endocrinology, 135, 2045- 2057.
  • Tilly, B. C., Mancini, G. M., Bijman, J., van Gageldonk, P. G., Beerens, C. E., Bridges, R. J., de Jonge, H. R. and Verheijen, F. W., 1992, Nucleotide-activated chloride channels in lysosomal membranes. Biochemical and Biophysical Research Communica- tions, 187, 254 - 260.
  • Tonini, R., Ferroni, A., Valenzuela, S. M., Warton, K., Campbell, T. J., Breit, S. N. and Mazzanti, M., 2000, Functional characterization of the NCC27 nuclear protein in stable transfected CHO-K1 cells. FASEB Journal, 14, 1171- 1178.
  • Tulk, B. M., Kapadia, S. and Edwards, J. C., 2002, CLIC1 inserts from the aqueous phase into phospholipid membranes, where it functions as an anion channel. American Journal of Physiology, 282, C1103 - C1112.
  • Tulk, B. M., Schlesinger, P. H., Kapadia, S. A. and Edwards, J. C., 2000, CLIC-1 functions as a chloride channel when expressed and purified from bacteria. Journal of Biological Chemistry, 275, 26986- 26993.
  • Valenzuela, S. M., Martin, D. K., Por, S. B., Robbins, J. M., Warton, K., Bootcov, M. R., Schofield, P. R., Campbell, T. J. and Breit, S. N., 1997, Molecular cloning and expression of a chloride ion channel of cell nuclei. Journal of Biological Chemistry, 272, 12575- 12582.
  • Valenzuela, S. M., Mazzanti, M., Tonini, R., Qiu, M. R., Warton, K., Musgrove, E. A., Campbell, T. J. and Breit, S. N., 2000, The nuclear chloride ion channel NCC27 is involved in regulation of the cell cycle. Journal of Physiology, 529, 541 - 552.
  • Valverde, M. A., Diaz, M., Sepulveda, F. V., Gill, D. R., Hyde, S. C. and Higgins, C. F., 1992, Volume-regulated chloride channels associated with the human multidrug-resistance P-glycoprotein. Nature, 355, 830 - 833.
  • Warton, K., Tonini, R., Fairlie, W. D., Matthews, J. M., Valenzuela, S. M., Qiu, M. R., Wu, W. M., Pankhurst, S., Bauskin, A. R., Harrop, S. J., Campbell, T. J., Curmi, P. M., Breit, S. N. and Mazzanti, M., 2002, Recombinant CLIC1 (NCC27) assembles in lipid bilayers via a pH-dependent two-state process to form chloride ion channels with identical characteristics to those observed in CHO cells expressing CLIC1. Journal of Biological Chemistry, 277, 26003- 26011.
  • Weber-Schurholz, S., Wischmeyer, E., Laurien, M., Jockusch, H., Schurholz, T., Landry, D. W. and Al-Awqati, Q., 1993, Indanylox- yacetic acid-sensitive chloride channels from outer membranes of skeletal muscle. Journal of Biological Chemistry, 268, 547 - 551. Weinreich, F. and Jentsch, T. J., 2001, Pores formed by single subunits in mixed dimers of different CLC chloride channels. Journal of Biological Chemistry, 276, 2347 - 2353.
  • Woodbury, D. J. and Miller, C., 1990, Nystatin-induced liposome fusion. A versatile approach to ion channel reconstitution into planar bilayers. Biophysical Journal, 58, 833 - 839.
  • Yin, Z. L., Dahlstrom, J. E., Le Couteur, D. G. and Board, P. G., 2001, Immunohistochemistry of omega class glutathione-S- transferase in human tissues. Journal of Histochemistry and Cytochemistry, 49, 983 - 987.
  • Zhou, X. W., Pfahnl, A., Werner, R., Hudder, A., Llanes, A., Luebke,A. and Dahl, G., 1997, Identification of a pore lining segment in gap junction hemichannels. Biophysical Journal, 72, 1946 - 1953. Zhou, Y., Morais-Cabral, J. H., Kaufman, A. and Mackinnon, R., 2001, Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 A0 resolution. Nature, 414, 43 - 48.

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