Crystal structure of a trimeric form of the KV7.1 (KCNQ1) A-domain tail coiled-coil reveals structural plasticity and context dependent changes in a putative coiled-coil trimerization motif

Protein Science

Volumn 18, Issue 10, 2009, Pages 2100-2114

  Xu, Qiang ^a   Minor Jr , Daniel L ^a,b,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Coiled coil; Kv7 (KCNQ) channel; Oligomeric assembly; R h x x h E motif

Indexed keywords

ION CHANNEL; POTASSIUM CHANNEL KCNQ1;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENERGY; HUMAN; OLIGOMERIZATION; PLASTICITY; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; HUMANS; KCNQ1 POTASSIUM CHANNEL; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; SEQUENCE ALIGNMENT; THERMODYNAMICS;

EID: 70349449896     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.224     Document Type: Article

References (74)

1. Woolfson DN (2005) The design of coiled-coil structures and assemblies. Adv Protein Chem 70:79-112.
2. Lupas AN, Gruber M (2005) The structure of alpha-helical coiled coils. Adv Protein Chem 70:37-78.
3. Grigoryan G, Keating AE (2008) Structural specificity in coiled-coil interactions. Curr Opin Struct Biol 18:477-483.
4. Testa OD, Moutevelis E, Woolfson DN (2009) CC+: a relational database of coiled-coil structures. Nucl Acids Res 37:D315-D322.
5. Crick FHC (1953) The packing of a-helices: simple coiled-coils. Acta Cryst 6:689-697.
6. Cohen C, Parry DAD (1990) a-helical coiled coils and bundles: how to design an a-helical protein. Proteins 7:1-15. (Pubitemid 20102598)
7. Parry DA, Fraser RD, Squire JM (2008) Fifty years of coiled-coils and alpha-helical bundles: a close relationship between sequence and structure. J Struct Biol 163:258-269.
8. Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252:1162-1164. (Pubitemid 21917026)
9. Wolf E, Kim PS, Berger B (1997) MultiCoil: a program for predicting two- and three-stranded coiled coils. Protein Sci 6:1179-1189. (Pubitemid 27260152)
10. Mcdonnell AV, Jiang T, Keating AE, Berger B (2006) Paircoil2: improved prediction of coiled coils from sequence. Bioinformatics 22:356-358. (Pubitemid 43205384)
11. Woolfson DN, Alber T (1995) Predicting oligomerization states of coiled coils. Protein Sci 4:1596-1607.
12. Conway JF, Parry DA (1991) Three-stranded alpha-fibrous proteins: the heptad repeat and its implications for structure. Int J Biol Macromol 13:14-16.
13. Conway JF, Parry DA (1990) Structural features in the heptad substructure and longer range repeats of two-stranded alpha-fibrous proteins. Int J Biol Macromol 12:328-334.
14. Harbury PB, Kim PS, Alber T (1994) Crystal structure of an isoleucine-zipper trimer. Nature 371:80-83.
15. Harbury PB, Zhang T, Kim PS, Alber T (1993) A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262:1401-1407. (Pubitemid 23983059)
16. Kammerer RA, Kostrewa D, Progias P, Honnappa S, Avila D, Lustig A, Winkler FK, Pieters J, Steinmetz MO (2005) A conserved trimerization motif controls the topology of short coiled coils. Proc Natl Acad Sci USA 102:13891-13896. (Pubitemid 41377674)
17. Gonzalez L, Woolfson DN, Alber T (1996) Buried polar residues and structural specificity in the GCN4 leucine zipper. Nat Struct Biol 3:1011-1018.
18. Beck K, Gambee JE, Kamawal A, Bachinger HP (1997) A single amino acid can switch the oligomerization state of the alpha-helical coiled-coil domain of cartilage matrix protein. EMBO J 16:3767-3777. (Pubitemid 27280992)
19. Liu J, Zheng Q, Deng Y, Kallenbach NR, Lu M (2006) Conformational transition between four and five-stranded phenylalanine zippers determined by a local packing interaction. J Mol Biol 361:168-179. (Pubitemid 44041450)
20. Yadav MK, Leman LJ, Price DJ, Brooks CL, Stout CD, Ghadiri MR (2006) Coiled coils at the edge of configurational heterogeneity. Structural analyses of parallel and antiparallel homotetrameric coiled coils reveal configurational sensitivity to a single solvent-exposed amino acid substitution. Biochemistry 45:4463-4473.
21. Yoder NC, Kumar K (2006) Selective protein-protein interactions driven by a phenylalanine interface. J Am Chem Soc 128:188-191. (Pubitemid 43100870)
22. Gonzalez L, Brown RA, Richardson D, Alber T (1996) Crystal structures of a single coiled-coil peptide in two oligomeric states reveal the basis for structural polymorphism. Nat Struct Biol 3:1002-1009. (Pubitemid 27014628)
23. Nautiyal S, Woolfson DN, King DS, Alber T (1995) A designed heterotrimeric coiled coil. Biochemistry 34:11645-11651.
24. Jenke M, Sanchez A, Monje F, Stuhmer W, Weseloh RM, Pardo LA (2003) C-terminal domains implicated in the functional surface expression of potassium channels. EMBO J 22:395-403. (Pubitemid 36193585)
25. Zhong H, Molday LL, Molday RS, Yau KW (2002) The heteromeric cyclic nucleotide-gated channel adopts a 3A:1B stoichiometry. Nature 420:193-198. (Pubitemid 35340125)
26. Syme CA, Hamilton KL, Jones HM, Gerlach AC, Giltinan L, Papworth GD, Watkins SC, Bradbury NA, Devor DC (2003) Trafficking of the Ca2+-activated K+ channel, hIK1, is dependent upon a C-terminal leucine zipper. J Biol Chem 278:8476-8486. (Pubitemid 36800599)
27. Howard RJ, Clark KA, Holton JM, Minor J, Daniel L (2007) Structural insight into KCNQ (Kv7) channel assembly and channelopathy. Neuron 53:663-675. (Pubitemid 46283377)
28. Tsuruda PR, Julius D, Minor DL (2006) Coiled coils direct assembly of a cold-activated TRP channel. Neuron 51:201-212 (Pubitemid 44041868)
29. Fujiwara Y, Minor DL, Jr (2008) X-ray crystal structure of a TRPM assembly domain reveals an antiparallel four-stranded coiled-coil. J Mol Biol 383:854-870.
30. Wiener R, Haitin Y, Shamgar L, Fernandez-Alonso MC, Martos A, Chomsky-Hecht O, Rivas G, Attali B, Hirsch JA (2008) The KCNQ1 (Kv7.1) COOH terminus, a multitiered scaffold for subunit assembly and protein interaction. J Biol Chem 283:5815-5830.
31. Lee SY, Letts JA, Mackinnon R (2008) Dimeric subunit stoichiometry of the human voltage-dependent proton channel Hv1. Proc Natl Acad Sci USA 105:7692-7695.
32. Celic A, Petri ET, Demeler B, Ehrlich BE, Boggon TJ (2008) Domain mapping of the polycystin-2 C-terminal tail using de novo molecular modeling and biophysical analysis. J Biol Chem 283:28305-28312.
33. Qian F, Germino FJ, Cai Y, Zhang X, Somlo S, Germino GG (1997) PKD1 interacts with PKD2 through a probable coiled-coil domain. Nat Genet 16:179-183. (Pubitemid 27240617)
34. Tsiokas L, Kim E, Arnould T, Sukhatme VP, Walz G (1997) Homo- and heterodimeric interactions between the gene products of PKD1 and PKD2. Proc Natl Acad Sci USA 94:6965-6970. (Pubitemid 27281974)
35. Haitin Y, Attali B (2008) The C-terminus of Kv7 channels: a multifunctional module. J Physiol 586:1803-1810. (Pubitemid 351997509)
36. Maljevic S, Lerche C, Seebohm G, Alekov AK, Busch AE, Lerche H (2003) C-terminal interaction of KCNQ2 and KCNQ3 K+ channels. J Physiol 548:353-360. (Pubitemid 36527459)
37. Schwake M, Athanasiadu D, Beimgraben C, Blanz J, Beck C, Jentsch TJ, Saftig P, Friedrich T (2006) Structural determinants of M-type KCNQ (Kv7) K+ channel assembly. J Neurosci 26:3757-3766.
38. Schwake M, Jentsch TJ, Friedrich T (2003) A carboxyterminal domain determines the subunit specificity of KCNQ K+ channel assembly. EMBO Rep 4:76-81. (Pubitemid 36305382)
39. Nakajo K, Kubo Y (2008) Second coiled-coil domain of KCNQ channel controls current expression and subfamily specific heteromultimerization by salt bridge networks. J Physiol 586:2827-2840. (Pubitemid 351837279)
40. Jespersen T, Grunnet M, Olesen SP (2005) The KCNQ1 potassium channel: from gene to physiological function. Physiology (Bethesda) 20:408-416. (Pubitemid 41812424)
41. Jentsch TJ (2000) Neuronal KCNQ potassium channels: physiology and role in disease. Nat Rev Neurosci 1:21-30.
42. Kurokawa J, Abriel H, Kass RS (2001) Molecular basis of the delayed rectifier current I(ks)in heart. J Mol Cell Cardiol 33:873-882. (Pubitemid 32545323)
43. Marx SO, Kurokawa J, Reiken S, Motoike H, D'armiento J, Marks AR, Kass RS (2002) Requirement for a macromolecular signaling complex for b adrenergic receptor modulation of the KCNQ1-KCNE1 potassium channel. Science 295:496-499. (Pubitemid 34101639)
44. Kass RS, Kurokawa J, Marx SO, Marks AR (2003) Leucine/isoleucine zipper coordination of ion channel macromolecular signaling complexes in the heart. Roles in inherited arrhythmias. Trends Cardiovasc Med 13:52-56.
45. Van Petegem F, Clark KA, Chatelain FC, Minor DL (2004) Structure of a complex between a voltage-gated calcium channel beta-subunit and an alpha-subunit domain. Nature 429:671-675.
46. Strelkov SV, Burkhard P (2002) Analysis of alpha-helical coiled coils with the program TWISTER reveals a structural mechanism for stutter compensation. J Struct Biol 137:54-64.
47. Lovell SC, Word JM, Richardson JS, Richardson DC (2000) The penultimate rotamer library. Proteins 40:389-408.
48. Neyroud N, Richard P, Vignier N, Donger C, Denjoy I, Demay L, Shkolnikova M, Pesce R, Chevalier P, Hainque B, Coumel P, Schwartz K, Guicheney P (1999) Genomic organization of the KCNQ1 K+ channel gene and identification of C-terminal mutations in the long-QT syndrome. Circ Res 84:290-297. (Pubitemid 29095569)
49. Dolenc J, Baron R, Missimer JH, Steinmetz MO, Van Gunsteren WF (2008) Exploring the conserved water site and hydration of a coiled-coil trimerisation motif: a MD simulation study. Chembiochem 9:1749-1756.
50. Kim JY, Kim MK, Kang GB, Park CS, Eom SH (2008) Crystal structure of the leucine zipper domain of small-conductance Ca2+-activated K+ (SK(Ca)) channel from Rattus norvegicus. Proteins 70:568-571.
51. Lumb KJ, Kim PS (1995) Measurement of interhelical electrostatic interactions in the GCN4 leucine zipper. Science 268:436-439.
52. Ibarra-Molero B, Zitzewitz JA, Matthews CR (2004) Salt-bridges can stabilize but do not accelerate the folding of the homodimeric coiled-coil peptide GCN4-p1. J Mol Biol 336:989-996. (Pubitemid 38229691)
53. Marti DN, Bosshard HR (2003) Electrostatic interactions in leucine zippers: thermodynamic analysis of the contributions of Glu and His residues and the effect of mutating salt bridges. J Mol Biol 330:621-637.
54. Grunnet M, Behr ER, Calloe K, Hofman-Bang J, Till J, Christiansen M, McKenna WJ, Olesen SP, Schmitt N (2005) Functional assessment of compound mutations in the KCNQ1 and KCNH2 genes associated with long QT syndrome. Heart Rhythm 2:1238-1249. (Pubitemid 41614170)
55. Kanki H, Kupershmidt S, Yang T, Wells S, Roden DM (2004) A structural requirement for processing the cardiac K+ channel KCNQ1. J Biol Chem 279:33976-33983. (Pubitemid 39063048)
56. Minor DL, Jr, Kim PS (1996) Context-dependent secondary structure formation of a designed protein sequence. Nature 380:730-734. (Pubitemid 26125475)
57. Cerasoli E, Sharpe BK, Woolfson DN (2005) ZiCo: a peptide designed to switch folded state upon binding zinc. J Am Chem Soc 127:15008-15009. (Pubitemid 41547351)
58. Pandya MJ, Cerasoli E, Joseph A, Stoneman RG, Waite E, Woolfson DN (2004) Sequence and structural duality: designing peptides to adopt two stable conformations. J Am Chem Soc 126:17016-17024. (Pubitemid 40069514)
59. Ambroggio XI, Kuhlman B (2006) Design of protein conformational switches. Curr Opin Struct Biol 16:525-530.
60. Ambroggio XI, Kuhlman B (2006) Computational design of a single amino acid sequence that can switch between two distinct protein folds. J Am Chem Soc 128:1154-1161.
61. Kapust RB, Tozser J, Fox JD, Anderson DE, Cherry S, Copeland TD, Waugh DS (2001) Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency. Protein Eng 14:993-1000. (Pubitemid 34137240)
62. Edelhoch H (1967) Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry 6:1948-1954.
63. Stoscheck CM (1990) Quantitation of protein. Methods Enzymol 182:50-68.
64. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41:207-234.
65. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326. (Pubitemid 27085611)
66. Terwilliger TC (2003) Solve and Resolve: automated structure solution and density modification. Methods Enzymol 374:22-37.
67. Langer G, Cohen SX, Lamzin VS, Perrakis A (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 3:1171-1179.
68. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126-2132. (Pubitemid 41742764)
69. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53:240-255.
70. Storoni LC, Mccoy AJ, Read RJ (2004) Likelihood-enhanced fast rotation functions. Acta Crystallogr D Biol Crystallogr 60:432-438.
71. Laskowski RA, Macarthur MW, Mosss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J App Cryst 26:283-291.
72. Delano WL (2002) The PyMOL molecular graphics system, San Carlos, CA: DeLano Scientific.
73. Brunger AT, Adams PD, Clore GM, Delano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54:905-921. (Pubitemid 28443603)
74. Chen YH, Yang JT, Chau KH (1974) Determination of the helix and beta form of proteins in aqueous solution by circular dichroism. Biochemistry 13:3350-3359.