Regulation of bestrophin Cl channels by calcium: Role of the C terminus

Journal of General Physiology

Volumn 132, Issue 6, 2008, Pages 681-692

  Xiao, Qinghuan ^a   Prussia, Andrew ^b   Yu, Kuai ^a   Cui, Yuan Yuan ^a   Hartzell, H Criss ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ASPARAGINE; ASPARTIC ACID; BESTROPHIN; CALCIUM; CALMODULIN; CHLORIDE CHANNEL; ELONGATION FACTOR 1; GLYCINE; MUTANT PROTEIN; TROPONIN C; UNCLASSIFIED DRUG; BEST1 PROTEIN, HUMAN; EYE PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM BINDING; CALCIUM SIGNALING; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; CRYSTAL STRUCTURE; HUMAN; HUMAN CELL; MATHEMATICAL COMPUTING; MOLECULAR BIOLOGY; MOLECULAR MODEL; MUTAGENESIS; PATCH CLAMP; POINT MUTATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; AMINO ACID SUBSTITUTION; CHEMICAL STRUCTURE; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN DOMAIN; PROTEIN MOTIF; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS; ULTRASTRUCTURE;

AMINO ACID SUBSTITUTION; CALCIUM; CHLORIDE CHANNELS; EF HAND MOTIFS; EYE PROTEINS; HUMANS; ION CHANNEL GATING; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN INTERACTION DOMAINS AND MOTIFS; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

EID: 59649115245     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.200810056     Document Type: Article

References (60)

1. 2+ sens- ing. J. Gen. Physiol. 123:475-489 .
2. Becke, A.D. 1993 . Density-functional thermochemistry. 3. The role of exact exchange. J. Phys. Chem. 98 : 5648 - 5652 .
3. Bian, S., I. Favre, and E. Moczydlowski . 2001 . Ca2+-binding activ- ity of a COOH-terminal fragment of the Drosophila BK channel involved in Ca2+-dependent activation. Proc. Natl. Acad. Sci. USA. 98 :4776-4781 .
4. Boys, S.F., and F . Bernardi . 1970 . Calculation of small molecular interactions by differences of separate total energies-some proce- dures with reduced errors. Mol. Phys. 19:553-566 .
5. Braun, A.P., and L. Sy . 2001 . Contribution of potential EF hand mo- tifs to the calcium-dependent gating of a mouse brain large con- ductance, calcium-sensitive K+ channel. J. Physiol. 533:681-695 .
6. Brose, N., K. Hofmann, Y . Hata, and T . C . Sudhof . 1995 . Mammalian homologues of Caenorhabditis elegans unc-13 gene def ne novel family of C(2)-domain proteins. J. Biol. Chem. 270:25273-25280 .
7. Burgess, R., I.D. Millar, B.P. Leroy, J.E. Urquhart, I.M. Fearon, B.E. De, P.D . Brown, A.G. Robson, G.A. Wright, P. Kestelyn, et al . 2008 . Biallelic mutation of BEST1 causes a distinct retinopathy in humans. Am. J. Hum. Genet. 82:19-31 .
8. Chattopadhyaya, R., W.E. Meador, A.R. Means, and F.A. Quiocho . 1992 . Calmodulin structure refned at 1.7 A resolution. J. Mol. Biol. 228 : 1177 - 1192 .
9. 2+ in Drosophila S2 cells are mediated by bestro- phins. J. Gen. Physiol. 128 : 247 - 259 .
10. Gifford J.L., M.P. Walsh, and H.J. Vogel . 2007 . Structures and metal-ion- binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. Biochem. J. 405 : 199 - 221 .
11. Guex, N., and M.C. Peitsch . 1997 . SWISS-MODEL and the Swiss- PdbViewer: an environment for comparative protein modeling. Electrophoresis . 18 : 2714 - 2723 .
12. Guziewicz, K.E., B. Zangerl, SJ. Lindauer, R.F. Mullins, L.S. Sandmeyer, B.H. Grahn, E.M. Stone, G.M. Acland, and G.D. Aguirre . 2007 . Bestrophin gene mutations cause canine multi- focal retinopathy: a novel animal model for best disease. Invest. Ophthalmol. Vis. Sci. 48 : 1959 - 1967 .
13. Hartzell, H.C, Z. Qu, K. Yu, Q. Xiao, and L.T. Chien . 2008 . Molecular physiology of bestrophins: multifunctional membrane proteins linked to best disease and other retinopathies. Physiol. Rev. 88 : 639 - 672 .
14. Hay, PJ., and W.R. Wadt . 1985 . Ab-initio effective core potentials for molecular calculations -potentials for K to Au including outermost pore orbitals. J. Chem. Phys. 82 : 299 - 310 .
15. Houdusse, A, and C. Cohen . 1996 . Structure of the regulatory domain of scallop myosin at 2 A resolution: implications for regulation. Structure . 4 : 21 - 32 .
16. Houdusse, A., M. Silver, and C. Cohen . 1996 . A model of Ca(2+)- free calmodulin binding to unconventional myosins reveals how calmodulin acts as a regulatory switch. Structure . 4 : 1475 - 1490 .
17. Jiang, Y, A. Lee, J. Chen, M. Cadene, B.T. Chait, and R. MacKinnon . 2002 . Crystal structure and mechanism of a calcium-gated potas- sium channel. Nature . 417 : 515 - 522 .
18. Jorgensen, W.L., and J. Tirado-Rives . 1988 . The OPLS potential func- tions for proteins-energy minimizations for crystals of cyclic-peptides and crambin. J. Am. Chem. Soc. 110 : 1657 - 1666 .
19. Kaminski, G., E.M. Duffy, T. Matsui, and W.L. Jorgensen . 1994 . Free energies of hydration and pure liquid properties of hydrocarbons from the OPLS all-atom model. J. Phys. Chem. 98 : 13077 - 13082 .
20. Kaminski, G., RA Friesner, J. Tirado-Rives, and W.L. Jorgensen . 2001 . Evaluation and reparametrization of the OPLS-AA force f eld for proteins via comparison with accurate quantum chemical calculations on peptides. J. Phys. Chem. 105 : 6474 - 6487 .
21. Lepsik, M., and MJ. Field . 2007 . Binding of calcium and other metal ions to the EF-hand loops of calmodulin studied by quantum chemical calculations and molecular dynamics simulations. J. Phys. Chem. B . 111 : 10012 - 10022 .
22. Lewit-Bentley, A., and S. Rety 2000 . EF-hand calcium-binding pro- teins. Curr. Opin. Struct. Biol. 10 : 637 - 643 .
23. Lingle, CJ. 2007 . Gating rings formed by RCK domains: keys to gate opening. J. Gen. Physiol. 129 : 101 - 107 .
24. Marquardt, A., H. Stohr, L.A Passmore, F. Kramer, A. Rivera, and B.H. Weber . 1998 . Mutations in a novel gene, VMD2, encoding a pro- tein of unknown properties cause juvenile-onset vitelliform macu- lar dystrophy (Best's disease). Hum. Mol. Genet. 7 : 1517 - 1525 .
25. Marten, B., K. Kim, C. Cortis, RA Friesner, and R. Murphy . 1996 . New model for calculation of solvation free energies: correction of self-consistent reaction f eld. J. Phys. Chem. 100 : 11775 - 11788 .
26. Maruyama, K., T. Mikawa, and S. Ebashi . 1984 . Detection of calcium binding proteins by 45Ca autoradiography on nitrocellulose mem- brane after sodium dodecyl sulfate gel electrophoresis. J. Biochem. (Tokyo) . 95 : 511 - 519 .
27. Nelson, M.R, and WJ. Chazin . 1998 . Structures of EF-hand Ca(2+)- binding proteins: diversity in the organization, packing and re- sponse to Ca2+ binding. Biometals . 11 : 297 - 318 .
28. Patton, C., S. Thompson, and D. Epel . 2004 . Some precautions in us- ing chelators to buffer metals in biological solutions. Cell Calcium. 35:427-431 .
29. Peitsch, M.C., T . N . Wells, D.R. Stampf, and J.L. Sussman . 1995 . The Swiss-3DImage collection and PDB-Browser on the World-Wide We b . Trends Biochem. Sci. 20:82-84 .
30. Petrukhin, K., M.J. Koisti, B. Bakall, W . Li, G. Xie, T . Marknell, O. Sandgren, K. Forsman, G. Holmgren, S. Andreasson, et al . 1998 . Identif cation of the gene responsible for Best macular dystrophy. Nat. Genet. 19:241-247 .
31. Pidcock, E., and G.R. Moore . 2001 . Structural characteristics of pro tein binding sites for calcium and lanthanide ions. J. Biol. Inorg. Chem. 6:479-489 .
32. 2+ . J. Gen. Physiol. 128:389-404 .
33. Qu, Z., L.T. Chien, Y . Cui, and H.C. Hartzell . 2006a . The anion- selective pore of the bestrophins, a family of chloride channels associated with retinal degeneration. J. Neurosci. 26:5411-5419 .
34. Qu, Z., Y. Cui, and C. Hartzell . 2006b . A short motif in the C-termi- nus of mouse bestrophin 4 inhibits its activation as a Cl channel. FEBS Lett. 580:2141-2146 .
35. Qu, Z., K. Yu, Y . Cui, C. Ying, and C. Hartzell . 2007 . Activation of be- strophin Cl channels is regulated by C-terminal domains. J. Biol. Chem. 282:17460-17467 .
36. Ravulapalli, R., B.G. Diaz, R.L. Campbell, and P.L. Davies . 2005 . Homodimerization of calpain 3 penta-EF-hand domain. Biochem. J. 388:585-591 .
37. Schreiber, M., and L. Salkoff . 1997 . A novel calcium-sensing domain in the BK channel. Biophys. J. 73 : 1355 - 1363 .
38. Schreiber, M., A. Yuan, and L. Salkoff . 1999 . Transplantable sites con- fer calcium sensitivity to BK channels. Nat. Neurosci. 2 : 416 - 421 .
39. Schwede, T ., J. Kopp, N. Guex, and M.C. Peitsch . 2003 . SWISS- MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385 .
40. Seddon, J.M., M.A. Afshari, S. Sharma, P.S. Bernstein, S. Chong, A. Hutchinson, K. Petrukhin, and R. Allikmets . 2001 . Assessment of mutations in the best macular dystrophy (VMD2) gene in pa- tients with adult-onset foveomacular vitelliform dystrophy, age- related maculopathy, and bull's-eye maculopathy. Ophthalmology. 108 : 2060 - 2067 .
41. Sheng, J.Z., A. Weljie, L. Sy, S. Ling, H.J. Vogel, and A.P. Braun . 2005 . Homology modeling identif es C-terminal residues that contribute to the Ca2+ sensitivity of a BKCa channel. Biophys. J. 89 : 3079 - 3092 .
42. + channels. J. Gen. Physiol. 118 : 589 - 606 .
43. Shi, J., G. Krishnamoorthy, Y . Ya n g, L. Hu, N. Chaturvedi, D. Harilal, J. Qin, and J. Cui . 2002 . Mechanism of magnesium activation of calcium-activated potassium channels. Nature . 418 : 876 - 880 .
44. Stanton, J.B., A.F. Goldberg, G. Hoppe, L.Y. Marmorstein, and A.D. Marmorstein . 2006 . Hydrodynamic properties of porcine bestro- phin-1 in Triton X-100. Biochim. Biophys. Acta . 1758 : 241 - 247 .
45. Stephens, P.J., FJ. Devlin, C.F. Chabalowski, and MJ. Frisch . 1994 . Ab-initio calculation of vibrational absorption and circular- dichroism spectra using density-functional force-f elds. J. Phys. Chem. 98 : 11623 - 11627 .
46. Still, W.C., A. Tempczyk, R.C. Hawley, and T. Hendrickson . 1990 . Semianalytical treatment of solvation for molecular mechanics and dynamics. J. Am. Chem. Soc. 112 : 6127 - 6129 .
47. Sun, H., T. Tsunenari, K.-W. Yau, and J. Nathans . 2002 . The vitelli- form macular dystrophy protein def nes a new family of chloride channels. Proc. Natl. Acad. Sci. USA . 99 : 4008 - 4013 .
48. Tannor, D.J., B. Marten, R. Murphy, R.A. Friesner, D. Sitkoff, A. Nicholls, M. Ringnalda, W.A. Goddard, and B. Honig . 1994 . Accurate first principles calculation of molecular charge- distributions and solvation energies from ab-initio quantum mechanics and continuum dielectric theory. J. Am. Chem. Soc. 116 : 11875 - 11882 .
49. Tsien, R.Y, and T. Pozzan . 1989 . Measurements of cytosolic free Ca2+ with Quin-2. Methods Enzymol. 172 : 230 - 262 .
50. 2+ -activated Cl- current from human bestrophin-4 in excised membrane patches. J. Gen. Physiol. 127 : 749 - 754 .
51. VanScyoc, W.S., R.A. Newman, B.R. Sorensen, and M.A. Shea . 2006 . Calcium binding to calmodulin mutants having domain- specif c effects on the regulation of ion channels. Biochemistry. 45 : 14311 - 14324 .
52. Xia, X.M., X. Zeng, and CJ. Lingle . 2002 . Multiple regulatory sites in large-conductance calcium-activated potassium channels. Nature . 418 : 880 - 884 .
53. Yang, W., H.W. Lee, H. Hellinga, and JJ. Yang . 2002 . Structural analysis, identif cation, and design of calcium-binding sites in proteins. Proteins . 47 : 344 - 356 .
54. Yap, K.L., J.B. Ames, M.B. Swindells, and M. Ikura . 1999 . Diversity of conformational states and changes within the EF-hand protein superfamily Proteins . 37 : 499 - 507 .
55. Yardley, J., B.P. Leroy, N. Hart-Holden, B.A. Lafaut, B. Loeys, L.M. Messiaen, R Perveen, M.A. Reddy, S.S. Bhattacharya, E. Traboulsi, et al . 2004 . Mutations of VMD2 splicing regulators cause nanoph- thalmos and autosomal dominant vitreoretinochoroidopathy (ADVIRC). Invest. Ophthalmol. Vis. Sci. 45 : 3683 - 3689 .
56. Yu, K., Y. Cui, and H.C. Hartzell . 2006 . The bestrophin mutation A243V, linked to adult-onset vitelliform macular dystrophy, im- pairs its chloride channel function. Invest. Ophthalmol. Vis. Sci. 47 : 4956 - 4961 .
57. Yu, K., Y. Cui, and H.C. Hartzell . 2007 . Chloride channel activity of bestrophin mutants associated with mild or late-onset macular degeneration. Invest. Ophthalmol. Vis. Sci. 48 : 4694 - 4705 .
58. Yusifov, T, N. Savalli, C.S. Gandhi, M. Ottolia, and R. Olcese . 2008 . The RCK2 domain of the human BKCa channel is a calcium sen- sor. Proc. Natl. Acad. Sci. USA . 105 : 376 - 381 .
59. 2+ through a nonselective, low aff nity divalent cation site. J. Gen. Physiol. 118 : 607 - 636 .
60. Zhou, Y, W. Yang, M. Kirberger, H.W. Lee, G. Ayalasomayajula, and JJ. Yang . 2006 . Prediction of EF-hand calcium-binding proteins and analysis of bacterial EF-hand proteins. Proteins . 65 : 643 - 655 .