Finding and characterizing tunnels in macromolecules with application to ion channels and pores

Biophysical Journal

Volumn 96, Issue 2, 2009, Pages 632-645

  Coleman, Ryan G ^a,b   Sharp, Kim A ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 58849142521     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.135970     Document Type: Article

References (68)

1. Bass, R. B., P. Strop, M. Barclay, and D. C. Rees. 2002. Crystal structure of Escherichia coli MscS, a voltage-modulated and mechanosensitive channel. Science. 298:1582-1587.
2. Moarefi, I., D. Jeruzalmi, J. Turner, M. O'Donnell, and J. Kurlyan. 2000. Crystal structure of the DNA polymerase processivity factor of T4 bacteriophage. J. Mol. Biol. 296:1215-1223.
3. Voss, N. R., M. Gerstein, T. A. Steitz, and P. B. Moore. 2006. The geometry of the ribosomal polypeptide exit tunnel. J. Mol. Biol. 360:893-906.
4. Roll-Mecak, A., and R. D. Vale. 2008. Structural basis of microtubule severing by the hereditary spastic paraplegia protein spastin. Nature. 451:363-367.
5. Taylor, T. C., and I. Andersson. 1997. The structure of the complex between rubisco and its natural substrate ribulose 1,5-bisphosphate. J. Mol. Biol. 265:432-444.
6. Gilson, M. K., T. P. Straatsma, J. A. McCammon, D. R. Ripoli, C. H. Faerman, et al. 1994. Open ''back door'' in a molecular dynamics simulation of acetylcholinesterase. Science. 263:1276-1278.
7. Murray, J. W., and J. Barber. 2007. Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel. J. Struct. Biol. 159:228-237.
8. White, S. H. 2007. Membrane proteins of known structure. http://blanco.biomol.uci.edu/Membrane-Proteins-xtal.html.
9. Hankamer, B., R. Glaeser, and H. Stahlberg. 2007. Electron crystallography of membrane proteins. J. Struct. Biol. 160:263-264.
10. Walian, P., T. A. Cross, and B. K. Jap. 2004. Structural genomics of membrane proteins. Genome Biol. 5:215.
11. White, S. H. 2004. The progress of membrane protein structure determination. Protein Sci. 13:1948-1949.
12. Bansal, A., and R. Sankararamakrishnan. 2007. Homology modeling of major intrinsic proteins in rice, maize and Arabidopsis: comparative analysis of transmembrane helix association and aromatic/arginine selectivity filters. BMC Struct. Biol. 7:27.
13. Smart, O. S., J. G. Neduvelil, X. Wang, B. A. Wallace, and M. S. P. Sansom. 1996. HOLE: A program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graph. 14:354-360.
14. Kelyweght, G. J., and T. A. Jones. 1994. Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallogr. D Biol. Crystallogr. 50:178-185.
15. Damborský, J., M. Petřek, P. Banáš, and M. Otyepka. 2007. Identification of tunnels in proteins, nucleic acids, inorganic materials and molecular ensembles. Biotechnol. J. 2007:62-67.
16. Petrek, M., M. Otyepka, P. Banáš, P. Košinová , J. Koča, et al. 2006. CAVER: A new tool to explore routes from protein clefts, pockets and cavities. BMC Bioinformatics. 7:1-9.
17. Lomize, M. A., A. L. Lomize, I. D. Pogozheva, and H. I. Mosberg. 2006. OPM: orientations of proteins in membranes database. Bioinformatics. 22:623-625.
18. Coleman, R. G., and K. A. Sharp. 2006. Travel depth, a new shape descriptor for macromolecules: application to ligand binding. J. Mol. Biol. 362:441-458.
19. Dijkstra, E. W. 1959. A note on two problems in connexion with graphs. Numerische Mathematik. 1:269-271.
20. Cormen, T. H., C. E. Leiserson, R. L. Rivest, and C. Stein. 2001. Introduction to Algorithms, 2nd ed. McGraw-Hill Higher Education, New York.
21. Feldman, J., and M. Singh. 2006. Bayesian estimation of the shape skeleton. Proc. Natl. Acad. Sci. USA. 103:18014-18019.
22. Larn, L., S.-W. Lee, and C. Y. Suen. 1992. Thinning methodologies- a comprehensive survey. IEEE Trans. Patt. Anal. and Mach. Intel. 14:869-885.
23. Reinders, F., M. E. D. Jacobson, and F. H. Post. 2000. Skeleton graph generation for feature shape description. Eurographics-IEEE TCVG Symposium on Visualization. 73-82.
24. Foskey, M., M. C. Lin, and D. Manocha. 2003. Efficient computation of a simplified medial axis. J. Comput. Inf. Sci. Eng. 3:274-284.
25. Nicholls, A., K. Sharp, and B. Honig. 1991. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins Struct. Funct. Genet. 4:281-296.
26. Bondi, A. 1964. van der Waals volumes and radii. J. Phys. Chem. 68:441-451.
27. Barber, C., D. Dobkin, and H. Huhdanpaa. 1993. The Quickhull algorithm for convex hull. In: Geometry Center Technical Report GCG53. University of Minnesota, Minneapolis.
28. Coleman, R. G. 2004. Finding knotted and linked vorticity lines in 3D vector fields. Master's Thesis. Tufts University, Medford, Massachusetts.
29. Wang, R., X. Fang, Y. Lu, and S. Wang. 2004. The PDBbind database: collection of binding affinities for protein-ligand complexes with known three-dimensional structures. J. Med. Chem. 47:2977-2980.
30. Wang, R., X. Fang, Y. Lu, C.-Y. Yang, and S. Wang. 2005. The PDBbind database: methodologies and updates. J. Med. Chem. 48:4111-4119.
31. Mardia, K. V. 1975. Statistics of directional data. J Roy Stat Soc B Method. 37:349-393.
32. Lundstrom, K. 2006. Structural genomics for membrane proteins. Cell. Mol. Life Sci. 63:2597-2607.
33. Nikaido, H. 2003. Molecular basis of bacterial outer membrane permeability. Microbiol. Mol. Biol. Rev. 67:593-656.
34. Koebnik, R., K. P. Locher, and P. Van Gelder. 2000. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 37:239-253.
35. Weiss, M.S., and G. E. Schulz. 1992. Structure of porinrefined at 1.8 A resolution. J. Mol. Biol. 227:493-509.
36. Kreusch, A., A. Neubüser, E. Schiltz, J. Weckesser, and G. E. Schulz. 1994. Structure of the membrane channel porin from Rhodopseudomonas at 2.0 Å resolution. Protein Sci. 3:58-63.
37. Dutzler, R., G. Rummel, S. Albertí, S. Hernández- Allés, P. Phale, et al. 1999. Crystal structure and functional characterization of OmpK36, the osmoporin of. Klebsiella pneumoniae. Structure. 7:425-434.
38. Zeth, K., K. Diederichs, W. Welte, and H. Engelhardt. 2000. Crystal structure of Omp32, the anion-selective porin from Comamonas acidovorans, in complex with a periplasmic peptide at 2.1 Å resolution. Structure. 8:981-992.
39. Zachariae, U., T. Klühspies, S. De, H. Engelhardt, and K. Zeth. 2006. High resolution crystal structures and molecular dynamics studies reveal substrate binding in the porin Omp32. J. Biol. Chem. 281:7413-7420.
40. Cowan, S. W., T. Schirmer, G. Rummel, M. Steiert, R. Ghosh, et al. 1992. Crystal structures explain functional properties of two E. coli porins. Nature. 358:727-733.
41. Baslé, A., G. Rummel, P. Storic, J. Rosenbusch, and T. Schirmer. 2006. Crystal structure of osmoporin OmpC from E. coli at 2.0 Å. J. Mol. Biol. 362:933-942.
42. Subbarao, G. V., and B. van der Berg. 2006. Crystal structure of the monomeric porin OmpG. J. Mol. Biol. 360:750-759.
43. Yildiz, O., K. R. Vinothkumar, P. Goswami, and W. Kühlbrandt. 2006. Structure of the monomeric outer-membrane porin OmpG in the open and closed confirmation. EMBO J. 25:3702-3713.
44. Meyer, J. E., M. Hofnung, and G. E. Schulz. 1997. Structure of maltoporin from Salmonella typhimurium ligated with a nitrophenyl-malto-trioside. J. Mol. Biol. 266:761-775.
45. Schirmer, T., T. A. Keller, Y. F. Wang, and J. Rosenbusch. 1995. Structural basis for sugar translocation through maltoporin channels at 3.1 Å resolution. Science. 267:512-514.
46. Forst, D., W. Welte, T. Wacker, and K. Diederichs. 1998. Structure of the sucrose-specific porin ScrY from Salmonella typhimurium and its complex with sucrose. Nat. Struct. Biol. 5:37-46.
47. Moraes, T. F., M. Bains, R. E. Hancock, and N. C. Strydnadka. 2007. An arginine ladder in OprP mediates phosphate-specific transfer across the outer membrane. Nat. Struct. Mol. Biol. 14:85-87.
48. Hedfalk, K., S. Törnroth-Horsefield, M. Nyblom, U. Johanson, P. Kjell-bom, et al. 2006. Aquaporin gating. Curr. Opin. Struct. Biol. 16:447-456.
49. Sui, H., B. G. Han, J. K. Lee, P. Walian, and B. K. Jap. 2001. Structural basis of water-specific transport through the AQP1 water channel. Nature. 414:872-878.
50. Lomize, A. L., I. D. Pogozheva, M. A. Lomize, and H. I. Mosberg. 2006. Positioning of proteins in membranes: a computational approach. Protein Sci. 15:1318-1333.
51. Senes, A., D. C. Chadi, P. B. Law, R. F. S. Walters, V. Nanda, et al. 2007. Ez, a depth-dependent potential for assessing the energies of insertion of amino acid side-chains into membranes: derivation and applications to determining the orientation of transmembrane and interfacial helices. J. Mol. Biol. 366:436-448.
52. Choe, S., K. A. Hecht, and M. Grabe. 2008. A continuum method for determining membrane protein insertion energies and the problem of charged residues. J. Gen. Physiol. 131:563-573.
53. Dunbrack, R. L., Jr., and G. Wang. 2003. PISCES: a protein sequence culling server. Bioinformatics. 19:1589-1591.
54. Yau, W.-M., W. C. Wimley, K. Gawrisch, and S. H. White. 1998. The preference of tryptophan for membrane interfaces. Biochemistry. 37:14713-14718.
55. Wiener, M. C., and S. H. White. 1992. Structure of a fluid dioleoylphos-phatidylcholine bilayer determined by joint refinement of x-ray and neutron diffraction data. III. Complete structure. Biophys. J. 61: 434-447.
56. Wallace, I. S., and D. M. Roberts. 2004. Homology modeling of representative subfamilies of arabidopsis major intrinsic proteins. classification based on the aromatic/arginine selectivity filter. Plant Physiol. 135:1029-1068.
57. Hille, B. 1992. Ionic Channels of Excitable Membranes. Sinauer Associates, Sunderland, Massachusetts.
58. Chen, H., F. Sesti, and S. A. N. Goldstein. 2003. Pore- and state-dependent cadmium block of IKs channels formed with MinK-55C and wild-type KCNQ1 subunits. Biophys. J. 84:3679-3689.
59. + channel allows inactivation to be modulated by metal binding. Biophys. J. 66:1068-1075.
60. Gross, A., and W. L. Hubbell. 2002. Identification of protein side chains near the membrane-aqueous interface: a site-directed spin labeling study of KcsA. Biochemistry. 41:1123-1128.
61. Pathak, M., L. Kurtz, F. Tombola, and E. Isacoff. 2004. The cooperative voltage sensor motion that gates a potassium channel. J. Gen. Physiol. 125:57-69.
62. Akiba, T., C. Toyoshima, T. Matsunaga, M. Kawamoto, T. Kubota, et al. 1996. Three-dimensional structure of bovine cytochrome bC1 complex by electron cryomicroscopy and helical image reconstruction. Nat. Struct. Biol. 3:553-561.
63. Beckstein, O., and M. S. P. Sansom. 2004. The influence of geometry, surface character and flexibility on the permeation of ions and waters through biological pores. Phys. Biol. 1:42-52.
64. Nagle, J. F., and H. J. Morowitz. 1978. Molecular mechanisms for proton transport in membranes. Proc. Natl. Acad. Sci. USA. 75:298-302.
65. Edelsbrunner, H., and E. P. Mücke. 1994. Three-dimensional alpha-shapes. ACM Trans. Graph. 13:43-72.
66. Kazhdan, M., T. Funkhouser, and S. Rusinkeiwicz. 2003. Rotation invariant spherical harmonic representation of 3D shape descriptors. Symp. Geom. Proc. 167-175.
67. Rahi, S. J., and K. A. Sharp. 2007. Mapping complicated surfaces onto a sphere. Int. J. Comput. Geom. Appl. 17:305-329.
68. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, California.