Regulation of the transient receptor potential channel TRPA1 by its N-terminal ankyrin repeat domain

Journal of Molecular Modeling

Volumn 19, Issue 11, 2013, Pages 4689-4700

  Zayats, Vasilina ^a,b   Samad, Abdul ^a   Minofar, Babak ^a,b   Roelofs, Katherine E ^c   Stockner, Thomas ^d   Ettrich, Rudiger ^a,b  

^a INSTITUTE OF MATHEMATICS   (Czech Republic)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^c PRINCETON UNIVERSITY   (United States)

^d MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Ankyrin repeat; EF hand; Familial episodic pain syndrom; TRPA1

Indexed keywords

ANKYRIN; CALCIUM BINDING PROTEIN; CALCIUM ION; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1;

AMINO TERMINAL SEQUENCE; ARTICLE; CALCIUM BINDING; CALCIUM CELL LEVEL; CRYOELECTRON MICROSCOPY; HAIR CELL; HUMAN; INTERPERSONAL COMMUNICATION; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NOCICEPTIVE PAIN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; SIGNAL TRANSDUCTION;

VERTEBRATA;

ANKYRIN REPEAT; BINDING SITES; CALCIUM; CALCIUM CHANNELS; EF HAND MOTIFS; HUMANS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; NERVE TISSUE PROTEINS; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 84888289833     PISSN: 16102940     EISSN: 09485023     Source Type: Journal    
DOI: 10.1007/s00894-012-1505-1     Document Type: Article

References (79)

1. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW et al. (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819-829
2. Corey DP, García-Añoveros J, Holt JR, Kwan KY, Lin SY, Vollrath MA, Amalfitano A, Cheung ELM, Derfler BH, Duggan A et al. (2004) TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432:723-730
3. Gaudet R (2008) A primer on ankyrin repeat function in TRP channels and beyond. Mol Biosyst 4:372-379
4. Sotomayor M, Corey DP, Schulten K (2005) In search of the hair-cell gating spring elastic properties of ankyrin and cadherin repeats. Structure 13:669-682
5. García-Añoveros J, Nagata K (2007) TRPA1. Handbook of experimental pharmacology. doi:10.1007/978-3-540-34891-7-21
6. Hinman A, Chuang HH, Bautista DM, Julius D (2006) TRP channel activation by reversible covalent modification. Proc Natl Acad Sci USA 103:19564-19568
7. Lux SE, John KM, Bennett V (1990) Analysis of cDNA for human erythrocyte ankyrin indicates a repeated structure with homology to tissue-differentiation and cell-cycle control proteins. Nature 344:36-42
8. Breeden L, Nasmyth K (1987) Similarity between cell-cycle genes of budding yeast and fission yeast and the Notch gene of Drosophila. Nature 329:651-654
9. Lee G, Abdi K, Jiang Y, Michaely P, Bennett V, Marszalek PE (2006) Nanospring behaviour of ankyrin repeats. Nature 440:246-249
10. Cavanaugh EJ, Simkin D, Kim D (2008) Activation of transient receptor potential A1 channels by mustard oil, tetrahydrocannabinol and Ca2+ reveals different functional channel states. Neuroscience 154:1467-1476
11. Macpherson LJ, Dubin AE, Evans MJ, Marr F, Schultz PG, Cravatt BF, Patapoutian A (2007) Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445:541-545
12. Sawada Y, Hosokawa H, Matsumura K, Kobayashi S (2008) Activation of transient receptor potential ankyrin 1 by hydrogen peroxide. Eur J Neurosci 27:1131-1142
13. Taylor-Clark TE, Kiros F, Carr MJ, McAlexander MA (2009) Transient receptor potential ankyrin 1 mediates toluene diisocyanate-evoked respiratory irritation. Am J Resp Cell Mol 40:756-762
14. Birrell MA, Belvisi MG, Grace M, Sadofsky L, Faruqi S, Hele DJ, Maher SA, Freund-Michel V, Morice AH (2009) TRPA1 agonists evoke coughing in guinea pig and human volunteers. Am J Respir Crit Care 180:1042-1047
15. Taylor-Clark TE, Undem BJ (2010) Ozone activates airway nerves via the selective stimulation of TRPA1 ion channels. J Physiol 588:423-433
16. Bessac BF, Sivula M, von Hehn CA, Caceres AI, Escalera J, Jordt SE (2009) Transient receptor potential ankyrin 1 antagonists block the noxious effects of toxic industrial isocyanates and tear gases. FASEB J 23:1102-1114
17. Doerner JF, Gisselmann G, Hatt H, Wetzel CH (2007) Transient receptor potential channel A1 is directly gated by calcium ions. J Biol Chem 282:13180-9
18. Zurborg S, Yurgionas B, Jira JA, Caspani O, Heppenstall PA (2007) Direct activation of the ion channel TRPA1 by Ca2+. Nat Neurosci 10:277-279
19. Kim D, Cavanaugh EJ, Simkin D (2008) Inhibition of transient receptor potential A1 channel by phosphatidylinositol-4,5-bisphosphate. Am J Physiol Cell Ph 295:C92-99
20. Dai Y, Wang S, Tominaga M, Yamamoto S, Fukuoka T, Higashi T, Kobayashi K, Obata K, Yamanaka H, Noguchi K (2007) Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J Clin Invest 117:1979-1987
21. Li L, Wetzel S, Plückthun A, Fernandez JM (2006) Stepwise unfolding of ankyrin repeats in a single protein revealed by atomic force microscopy. Biophys J 90:L30-2
22. Serquera D, Lee W, Settanni G, Marszalek PE, Paci E, Itzhaki LS (2010) Mechanical unfolding of an ankyrin repeat protein. Biophys J 98:1294-1301
23. Michaely P, Tomchick DR, Machius M, Anderson RGW (2002) Crystal structure of a 12 ANK repeat stack from human ankyrinR. EMBO J 21:6387-6396
24. Rost B, Yachdav G, Liu J (2004) The predictprotein server. Nucleic Acids Res 32:W321-6
25. Söding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244-248
26. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinforma 9:40
27. Bennett-Lovsey RM, Herbert AD, Sternberg MJE, Kelley LA (2008) Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins 70:611-625
28. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R et al. (2007) ClustalW and ClustalX version 2. Bioinformatics 23:2947-2948
29. Sali A, Blundell TL (1993) Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 234:779-815
30. Korndörfer IP, Brueckner F, Skerra A (2007) The crystal structure of the human (S100A8/S100A9)2 heterotetramer, calprotectin, illustrates how conformational changes of interacting alpha-helices can determine specific association of two EF-hand proteins. J Mol Biol 370:887-898
31. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283-291
32. Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35:W407-10
33. Chen X, Wang Q, Ni F, Ma J (2010) Structure of the full-length Shaker potassium channel Kv1.2 by normal-mode-based X-ray crystallographic refinement. Proc Natl Acad Sci USA 107:11352-11357
34. Sonnhammer EL, von Heijne G, Krogh A (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6:175-182
35. Hofmann K, Stoffel W (1993) TMBASE - a database of membrane spanning protein segments. Biol Chem 374:166-170
36. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205-217
37. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 5:113
38. Krieger E, Koraimann G, Vriend G (2002) Increasing the precision of comparative models with YASARA NOVA-a self-parameterizing force field. Proteins 47:393-402
39. Berendsen HJC, Postma JPM, van Gunsteren WF, Hermans J (1981) In: Intermolecular Force. B. Pullman (ed.), Reidel, Dordrecht, pp 331-342
40. Hess B, Kutzner C, van der Spoel D, Lindahl E (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theor Comput 4:435-447
41. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJC (2005) GROMACS: fast, flexible, and free. J Comput Chem 26:1701-1718
42. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81:3684-3690
43. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18:1463-1472
44. Darden T, York D, Pedersen L (1993) Particle mesh Ewald: an N×log(N) method for Ewald sums in large systems. J Chem Phys 98:10089-10092
45. Kandt C, Ash WL, Tieleman DP (2007) Setting up and running molecular dynamics simulations of membrane proteins. Methods 41:475-488
46. Berger O, Edholm O, Jahnig F (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys J 72:2002-2013.47
47. Jorgensen WL, Maxwell DS, Tirado-Rives J (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J Am Chem Soc 118:11225-11236
48. http://lists.gromacs.org/pipermail/gmx-developers/2008-March/002422.html and http://www.pomeslab.com/files/lipidCombinationRules.pdf
49. Nilius B, Owsianik G, Voets T (2008) Transient receptor potential channels meet phosphoinositides. EMBO J 27:2809-2816
50. Qin F (2007) Regulation of TRP ion channels by phosphatidylinositol-4,5- bisphosphate. Handbook of experimental pharmacology. doi:10.1007/978-3-540- 34891-7-30
51. Karashima Y, Prenen J, Meseguer V, Owsianik G, Voets T, Nilius B (2008) Modulation of the transient receptor potential channel TRPA1 by phosphatidylinositol 4,5-biphosphate manipulators. Pflügers Arch: E J Physiol 457:77-89
52. van Rossum DB, Patterson RL, Sharma S, Barrow RK, Kornberg M, Gill DL, Snyder SH (2005) Phospholipase Cgamma1 controls surface expression of TRPC3 through an intermolecular PH domain. Nature 434:99-104
53. Wen W, Yan J, Zhang M (2006) Structural characterization of the split pleckstrin homology domain in phospholipase C-gamma1 and its interaction with TRPC3. J Biol Chem 281:12060-8
54. Marchler-Bauer A, Panchenko AR, Shoemaker BA, Thiessen PA, Geer LY, Bryant SH (2002) CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res 30:281-283
55. Haslam RJ, Koide HB, Hemmings BA (1993) Pleckstrin domain homology. Nature 363:309-310
56. Jia J, Borregaard N, Lollike K, Cygler M (2001) Structure of Ca(2+)-loaded human grancalcin. Acta Crystallogr D 57:1843-1849
57. Boehr DD, Nussinov R, Wright PE (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 5:789-796. doi: 10.1038/nchembio.232
58. Stockner T, Vogel HJ, Tieleman DP (2005) A salt-bridge motif involved in ligand binding and large-scale domain motions of the maltose-binding protein. Biophys J 89:3362-3371
59. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Högestätt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260-265
60. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849-857
61. Bautista DM, Movahed P, Hinman A, Axelsson HE, Sterner O, Högestätt ED, Julius D, Jordt SE, Zygmunt PM (2005) Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci USA 102:12248-12252
62. Nagata K, Duggan A, Kumar G, García-Añoveros J (2005) Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J Neurosci 25:4052-4061
63. Wang YY, Chang RB, Waters HN, McKemy DD, Liman ER (2008) The nociceptor ion channel TRPA1 is potentiated and inactivated by permeating calcium ions. J Biol Chem 283:32691-32703
64. Hu H, Bandell M, Petrus MJ, Zhu MX, Patapoutian A (2009) Zinc activates damage-sensing TRPA1 ion channels. Nature Chem Biol 5:183-190
65. Kremeyer B, Lopera F, Cox JJ, Momin A, Rugiero F, Marsh S, Woods CG, Jones NG, Paterson KJ, Fricker FR et al. (2010) A gain-of-function mutation in TRPA1 causes familial episodic pain syndrome. Neuron 66:671-680
66. Cvetkov TL, Huynh KW, Cohen MR, Moiseenkova-Bell VY (2011) Molecular architecture and subunit organization of TRPA1 channel revealed by electron microscopy. J Biol Chem 286:38168-38176
67. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera - a visualization system for exploratory research and analysis. J Comput Chem 25:1605-1612
68. Pintilie GD, Zhang J, Goddard TD, Chiu W, Gossard DC (2010) Quantitative analysis of cryo-EM density map segmentation by watershed and scale-space filtering, and fitting of structures by alignment to regions. J Struct Biol 170(3):427-438
69. Strawn R, Melichercik M, Green M, Stockner T, Carey J, Ettrich R (2010) Symmetric allosteric mechanism of hexameric Escherichia coli arginine repressor exploits competition between L-arginine ligands and resident arginine residues. PLoS Comput Biol 6(6):e1000801
70. Benedikt J, Samad A, Ettrich R, Teisinger J, Vlachova V (2009) Essential role for the putative S6 inner pore region in the activation gating of the human TRPA1 channel. Biochim Biophys Acta 1793:1279-88.72
71. Samad A, Sura L, Benedikt J, Ettrich R, Minofar B, Teisinger J, Vlachova V (2010) The C-terminal basic residues contribute to the chemical- and voltage-dependent activation of TRPA1. Biochem J 433:197-204
72. Wang L, Cvetkov TL, Chance MR, Moiseenkova-Bell VY (2012) Identification of in vivo disulfide conformation of TRPA1 ion channel. J Biol Chem 287:6169-6176
73. Hudspeth AJ, Corey DP (1977) Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. Proc Natl Acad Sci USA 74:2407-2411
74. Gillespie PG, Walker RG (2001) Molecular basis of mechanosensory transduction. Nature 413:194-202
75. Hudspeth AJ (1982) Extracellular current flow and the site of transduction by vertebrate hair cells. J Neurosci 2:1-10
76. Gillespie PG, Wagner MC, Hudspeth AJ (1993) Identification of a 120 kd hair-bundle myosin located near stereociliary tips. Neuron 11:581-94
77. García JA, Yee AG, Gillespie PG, Corey DP (1998) Localization of myosin-Ibeta near both ends of tip links in frog saccular hair cells. J Neurosci 18:8637-8647
78. Holt JR, Gillespie SKH, Provance DW, Shah K, Shokat KM, Corey DP, Mercer JA, Gillespie PG (2002) A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 108:371-381
79. Howard J, Hudspeth AJ (1988) Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell. Neuron 1:189-199