Regulatory phosphorylation induces extracellular conformational changes in a CLC anion channel

Biophysical Journal

Volumn 104, Issue 9, 2013, Pages 1893-1904

  Yamada, Toshiki ^a   Bhate, Manasi P ^b   Strange, Kevin ^a  

^a MOUNT DESERT ISLAND BIOLOGICAL LABORATORY   (United States)

^b Howard Hughes Medical Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE CHANNEL; CLC 3 CHANNEL; CLC-3 CHANNEL; PROTEIN SERINE THREONINE KINASE; SERINE;

AMINO ACID SEQUENCE; ARTICLE; CELL STRAIN HEK293; CHANNEL GATING; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; MUTATION; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; CHLORIDE CHANNELS; HEK293 CELLS; HUMANS; ION CHANNEL GATING; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SERINE;

EID: 84877249807     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.03.026     Document Type: Article

References (59)

1. R. Dutzler, E.B. Campbell, and R. MacKinnon Gating the selectivity filter in ClC chloride channels Science 300 2003 108 112
2. R. Dutzler, and E.B. Campbell R. MacKinnon X-ray structure of a ClC chloride channel at 3.0 A reveals the molecular basis of anion selectivity Nature 415 2002 287 294
3. L. Feng, and E.B. Campbell R. MacKinnon Structure of a eukaryotic CLC transporter defines an intermediate state in the transport cycle Science 330 2010 635 641
4. C. Duran, and C.H. Thompson H.C. Hartzell Chloride channels: often enigmatic, rarely predictable Annu. Rev. Physiol. 72 2010 95 121
5. T.J. Jentsch CLC chloride channels and transporters: from genes to protein structure, pathology and physiology Crit. Rev. Biochem. Mol. Biol. 43 2008 3 36
6. J.M. Cederholm, and G.Y. Rychkov A.H. Bretag Inter-subunit communication and fast gate integrity are important for common gating in hClC-1 Int. J. Biochem. Cell Biol. 42 2010 1182 1188
7. M. Duffield, and G. Rychkov M. Roberts Involvement of helices at the dimer interface in ClC-1 common gating J. Gen. Physiol. 121 2003 149 161
8. L. Ma, and G.Y. Rychkov A.H. Bretag Movement of hClC-1 C-termini during common gating and limits on their cytoplasmic location Biochem. J. 436 2011 415 428
9. E.A. Bykova, and X.D. Zhang J. Zheng Large movement in the C terminus of CLC-0 chloride channel during slow gating Nat. Struct. Mol. Biol. 13 2006 1115 1119
10. T. Furukawa, and T. Ogura N. Inagaki Phosphorylation and functional regulation of ClC-2 chloride channels expressed in Xenopus oocytes by M cyclin-dependent protein kinase J. Physiol. 540 2002 883 893
11. K.M. Hsiao, and R.Y. Huang M.J. Lin Functional study of CLC-1 mutants expressed in Xenopus oocytes reveals that a C-terminal region Thr891-Ser892-Thr893 is responsible for the effects of protein kinase C activator Cell. Physiol. Biochem. 25 2010 687 694
12. (-) channel J. Biol. Chem. 279 2004 21849 21856
13. D. Duan, and S. Cowley J.R. Hume A serine residue in ClC-3 links phosphorylation-dephosphorylation to chloride channel regulation by cell volume J. Gen. Physiol. 113 1999 57 70
14. N.C. Robinson, and P. Huang D.J. Nelson Identification of an N-terminal amino acid of the CLC-3 chloride channel critical in phosphorylation-dependent activation of a CaMKII-activated chloride current J. Physiol. 556 2004 353 368
15. B. Bennetts, M.W. Parker, and B.A. Cromer Inhibition of skeletal muscle ClC-1 chloride channels by low intracellular pH and ATP J. Biol. Chem. 282 2007 32780 32791
16. A. De Angeli, and O. Moran F. Gambale ATP binding to the C terminus of the Arabidopsis thaliana nitrate/proton antiporter, AtCLCa, regulates nitrate transport into plant vacuoles J. Biol. Chem. 284 2009 26526 26532
17. P.Y. Tseng, and W.P. Yu T.Y. Chen Binding of ATP to the CBS domains in the C-terminal region of CLC-1 J. Gen. Physiol. 137 2011 357 368
18. J.W. Scott, and S.A. Hawley D.G. Hardie CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations J. Clin. Invest. 113 2004 274 284
19. S. Meyer, and S. Savaresi R. Dutzler Nucleotide recognition by the cytoplasmic domain of the human chloride transporter ClC-5 Nat. Struct. Mol. Biol. 14 2007 60 67
20. L. Wellhauser, and C. Luna-Chavez C.E. Bear ATP binding induces conformational changes in the carboxy terminal region of ClC-5 J. Biol. Chem. 268 2011 6733 6741
21. B. Bennetts, and Y. Yu M.W. Parker Intracellular β-nicotinamide adenine dinucleotide inhibits the skeletal muscle ClC-1 chloride channel J. Biol. Chem. 287 2012 25808 25820
22. E. Jeworutzki, and T. López-Hernández R. Estévez GlialCAM, a protein defective in a leukodystrophy, serves as a ClC-2 Cl(-) channel auxiliary subunit Neuron 73 2012 951 961
23. +)-exchanger and requires Ostm1 for transport activity EMBO J. 30 2011 2140 2152
24. M. Fischer, A.G. Janssen, and C. Fahlke Barttin activates ClC-K channel function by modulating gating J. Am. Soc. Nephrol. 21 2010 1281 1289
25. U. Scholl, and S. Hebeisen C. Fahlke Barttin modulates trafficking and function of ClC-K channels Proc. Natl. Acad. Sci. USA 103 2006 11411 11416
26. A. Gradogna, and E. Babini M. Pusch A regulatory calcium-binding site at the subunit interface of CLC-K kidney chloride channels J. Gen. Physiol. 136 2010 311 323
27. A. Gradogna, and C. Fenollar-Ferrer M. Pusch Dissecting a regulatory calcium-binding site of CLC-K kidney chloride channels J. Gen. Physiol. 140 2012 681 696
28. E. Rutledge, and L. Bianchi K. Strange CLH-3, a ClC-2 anion channel ortholog activated during meiotic maturation in C. elegans oocytes Curr. Biol. 11 2001 161 170
29. E. Rutledge, J. Denton, and K. Strange Cell cycle- and swelling-induced activation of a Caenorhabditis elegans ClC channel is mediated by CeGLC-7α/β phosphatases J. Cell Biol. 158 2002 435 444
30. R.A. Falin, and R. Morrison K. Strange Identification of regulatory phosphorylation sites in a cell volume- and Ste20 kinase-dependent ClC anion channel J. Gen. Physiol. 133 2009 29 42
31. J. Denton, and K. Nehrke K. Strange GCK-3, a newly identified Ste20 kinase, binds to and regulates the activity of a cell cycle-dependent ClC anion channel J. Gen. Physiol. 125 2005 113 125
32. R.A. Falin, H. Miyazaki, and K. Strange C. elegans STK39/SPAK ortholog-mediated inhibition of ClC anion channel activity is regulated by WNK-independent ERK kinase signaling Am. J. Physiol. Cell Physiol. 300 2011 C624 C635
33. E. Delpire, and K.B. Gagnon SPAK and OSR1: STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells Biochem. J. 409 2008 321 331
34. H. Miyazaki, and T. Yamada K. Strange CLC anion channel regulatory phosphorylation and conserved signal transduction domains Biophys. J. 103 2012 1706 1718
35. S. Ignoul, and J. Eggermont CBS domains: structure, function, and pathology in human proteins Am. J. Physiol. Cell Physiol. 289 2005 C1369 C1378
36. A.A. Baykov, H.K. Tuominen, and R. Lahti The CBS domain: a protein module with an emerging prominent role in regulation ACS Chem. Biol. 6 2011 1156 1163
37. R. Townley, and L. Shapiro Crystal structures of the adenylate sensor from fission yeast AMP-activated protein kinase Science 315 2007 1726 1729
38. X. Jin, R. Townley, and L. Shapiro Structural insight into AMPK regulation: ADP comes into play Structure 15 2007 1285 1295
39. 2+ transporter Nature 448 2007 1072 1075
40. N.A. Mahmood, E. Biemans-Oldehinkel, and B. Poolman Engineering of ion sensing by the cystathionine beta-synthase module of the ABC transporter OpuA J. Biol. Chem. 284 2009 14368 14376
41. M.D. Duffield, and G.Y. Rychkov M.L. Roberts Zinc inhibits human ClC-1 muscle chloride channel by interacting with its common gating mechanism J. Physiol. 568 2005 5 12
42. T.Y. Chen Extracellular zinc ion inhibits ClC-0 chloride channels by facilitating slow gating J. Gen. Physiol. 112 1998 715 726
43. Y.W. Lin, C.W. Lin, and T.Y. Chen Elimination of the slow gating of ClC-0 chloride channel by a point mutation J. Gen. Physiol. 114 1999 1 12
44. H. Miyazaki, and K. Strange Differential regulation of a CLC anion channel by SPAK kinase ortholog-mediated multisite phosphorylation Am. J. Physiol. Cell Physiol. 302 2012 C1702 C1712
45. L. He, and J. Denton K. Strange Carboxy terminus splice variation alters ClC channel gating and extracellular cysteine reactivity Biophys. J. 90 2006 3570 3581
46. M. Pusch, and U. Ludewig T.J. Jentsch Gating of the voltage-dependent chloride channel CIC-0 by the permeant anion Nature 373 1995 527 531
47. M.F. Chen, and T.Y. Chen Side-chain charge effects and conductance determinants in the pore of ClC-0 chloride channels J. Gen. Physiol. 122 2003 133 145
48. T.Y. Chen, M.F. Chen, and C.W. Lin Electrostatic control and chloride regulation of the fast gating of ClC-0 chloride channels J. Gen. Physiol. 122 2003 641 651
49. R.E. Middleton, D.J. Pheasant, and C. Miller Homodimeric architecture of a ClC-type chloride ion channel Nature 383 1996 337 340
50. S. Lourdel, and T. Grand J. Teulon ClC-5 mutations associated with Dent's disease: a major role of the dimer interface Pflugers Arch. 463 2012 247 256
51. M. Pusch Myotonia caused by mutations in the muscle chloride channel gene CLCN1 Hum. Mutat. 19 2002 423 434
52. A.A. Zamyatnin Protein volume in solution Prog. Biophys. Mol. Biol. 24 1972 107 123
53. L. Zúñiga, and M.I. Niemeyer F.V. Sepúlveda The voltage-dependent ClC-2 chloride channel has a dual gating mechanism J. Physiol. 555 2004 671 682
54. B. Bennetts, and M.L. Roberts G.Y. Rychkov Temperature dependence of human muscle ClC-1 chloride channel J. Physiol. 535 2001 83 93
55. C. Saviane, F. Conti, and M. Pusch The muscle chloride channel ClC-1 has a double-barreled appearance that is differentially affected in dominant and recessive myotonia J. Gen. Physiol. 113 1999 457 468
56. B. Bennetts, and G.Y. Rychkov B.A. Cromer Cytoplasmic ATP-sensing domains regulate gating of skeletal muscle ClC-1 chloride channels J. Biol. Chem. 280 2005 32452 32458
57. P.Y. Tseng, B. Bennetts, and T.Y. Chen Cytoplasmic ATP inhibition of CLC-1 is enhanced by low pH J. Gen. Physiol. 130 2007 217 221
58. Y.R. Yusef, and L. Zúñiga F.V. Sepúlveda Removal of gating in voltage-dependent ClC-2 chloride channel by point mutations affecting the pore and C-terminus CBS-2 domain J. Physiol. 572 2006 173 181
59. A. Accardi, and M. Pusch Conformational changes in the pore of CLC-0 J. Gen. Physiol. 122 2003 277 293