3D structure of the skeletal muscle dihydropyridine receptor

Journal of Molecular Biology

Volumn 323, Issue 1, 2002, Pages 85-98

  Wang, Ming Chuan ^a   Velarde, Giles ^a   Ford, Robert C ^a   Berrow, Nicholas S ^b   Dolphin, Annette C ^b   Kitmitto, Ashraf ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

3D reconstruction; Dihydropyridine receptor; Electron microscopy; L type voltage gated calcium; Negative staining

Indexed keywords

1,4 DIHYDROPYRIDINE RECEPTOR; CALCIUM CHANNEL;

ARTICLE; CHROMATOGRAPHY; ELECTRON MICROSCOPY; IMMUNOBLOTTING; MOLECULAR INTERACTION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SKELETAL MUSCLE; STRUCTURE ANALYSIS;

EID: 0036396740     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)00890-2     Document Type: Article

References (61)

1. Hagiwara, S. & Byerly, L. (1981). Calcium channel. Annu. Rev. Neurosci. 4, 69-125.
2. Janis, R. A. & Triggle, D. J. (1984). 1,4-Dihydropyridine Ca-2+ channel antagonists and activators-a comparison of binding characteristics with pharmacology. Drug Dev. Res. 4, 257-274.
3. Rios, E. & Brum, G. (1987). Involvement of dihydropyridine receptors in excitation contraction coupling in skeletal-muscle. Nature, 325, 717-720.
4. Grabner, M., Dirksen, R. T., Suda, N. & Beam, K. G. (1999). The II-III loop of the skeletal muscle dihydropyridine receptor is responsible for the bi-directional coupling with the ryanodine receptor. J. Biol. Chem. 274, 21913-21919.
5. Wilkens, C. M., Kasielke, N., Flucher, B. E., Beam, K. G. & Grabner, M. (2001). Excitation-contraction coupling is unaffected by drastic alteration of the sequence surrounding residues L720-L764 of the alpha(1S) II-III loop. Proc. Natl Acad. Sci. USA, 98, 5892-5897.
6. Curtis, B. M. & Catterall, W. A. (1984). Purification of the calcium antagonist receptor of the voltage sensitive calcium channel from skeletal muscle transverse tubules. Biochemistry, 23, 2113-2118.
7. Sharp, A. H., Imagawa, T., Leung, A. T. & Campbell, K. P. (1987). Identification and characterization of the dihydropyridine-binding subunit of the skeletal-muscle dihydropyridine receptor. J. Biol. Chem. 262, 12309-12315.
8. Florio, V., Striessnig, J. & Catterall, W. A. (1992). Purification and reconstitution of skeletal-muscle calcium channels. Methods Enzymol. 207, 529-546.
9. Leung, A. T., Imagawa, T. & Campbell, K. P. (1987). Structural characterization of the 1,4-dihydropyridine receptor of the voltage-dependent Ca-2+ channel from rabbit skeletal-muscle-evidence for 2 distinct high-molecular-weight subunits. J. Biol. Chem. 262, 7943-7946.
10. Catterall, W. A. (1988). Structure and function of voltage-sensitive ion channels. Science, 242, 50-61.
11. Tanabe, T., Takeshima, H., Mikami, A., Flockerzi, V., Takahashi, H., Kangawa, K. et al. (1987). Primary structure of the receptor for calcium-channel blockers from skeletal-muscle. Nature, 328, 313-318.
12. Ellis, S. B., Williams, M., Ways, N. R., Brenner, R., Sharp, A. H., Leung, A. T. et al. (1988). Sequence and expression of messenger-RNAs encoding the alpha-1 subunit and alpha-2 subunit of DHP-sensitive calcium channel. Science, 241, 1661-1664.
13. De Jongh, K. S., Warner, C. & Catterall, W. A. (1990). Subunits of purified calcium channels-alpha-2 and delta are encoded by the same gene. J. Biol. Chem. 265, 14738-14741.
14. Jay, S. D., Sharp, A. H., Kahl, S. D., Vedvick, T. S., Harpold, M. M. & Campbell, K. P. (1991). Structural characterization of the dihydropyridine-sensitive calcium-channel alpha-2-subunit and the associated delta-peptides. J. Biol. Chem. 266, 3287-3293.
15. Brickley, K., Campbell, V., Berrow, N., Leach, R., Norman, R. I., Wray, D. et al. (1995). Use Of site-directed antibodies to probe the topography of the alpha(2) subunit of voltage-gated Ca2+ channels. FEBS Letters, 364, 129-133.
16. Gurnett, C. A., De Waard, M. & Campbell, K. P. (1996). Dual function of the voltage-dependent Ca2 + channel alpha(2)delta subunit in current stimulation and subunit interaction. Neuron, 16, 431-440.
17. Walker, D. & De Waard, M. (1998). Subunit interaction sites in voltage-dependent Ca2+ channels: role in channel function. Trends Neurosci. 21, 148-154.
18. Jay, S. D., Ellis, S. B., McCue, A. F., Willimas, M. E., Vedvick, T. S., Harpold, M. M. & Campbell, K. P. (1990). Primary structure of the gamma-subunit of the DHP-sensitive calcium-channel from skeletal muscle. Science, 248, 490-492.
19. Hofmann, F., Biel, M. & Flockerzi, V. (1994). Molecular-basis for Ca2+ channel diversity. Annu. Rev. Neurosci. 17, 399-418.
20. DeWaard, M., Scott, V. E. S., Pragnell, M. & Campbell, K. P. (1996). Identification of critical amino acids involved in alpha(1)-beta interaction in voltage-dependent Ca2+ channels. FEBS Letters, 380, 272-276.
21. Brice, N. L., Berrow, N. S., Campbell, V., Page, K. M., Brickley, K., Tedder, I. & Dolphin, A. C. (1997). Importance of the different beta subunits in the membrane expression of the alpha 1A and alpha 2 calcium channel subunits: studies using a depolarization-sensitive alpha 1A antibody. Eur. J. Neurosci. 9, 749-759.
22. Gurnett, C. A., Felix, R. & Campbell, K. P. (1997). Extracellular interaction of the voltage-dependent Ca2+ channel alpha(2)delta and alpha(1) subunits. J. Biol. Chem. 272, 18508-18512.
23. Gao, T., Chien, A. J. & Hosey, M. M. (1999). Complexes of the alpha(1C) and beta subunits generate the necessary signal for membrane targeting of class C L-type calcium channels. J. Biol. Chem. 274, 2137-2144.
24. Franzini-Armstrong, C. (1984). Freeze-fracture of frog slow tonic fibres:structure of surface and internal membranes. Tissue Cell, 16, 146-166.
25. Block, B. A., Imagawa, T., Leung, A., Campbell, P. & Franzini-Armstrong, C. (1988). Structural evidence for direct interaction between the molecular-components of the transverse tubule sarcoplasmic-reticulum junction in skeletal-muscle. J. Cell Biol. 107, 2587-2600.
26. Franzini-Armstrong, C. & Jorgenson, A. O. (1994). Structure and development of E-C coupling units in skeletal muscle. Annu. Rev. Physiol. 56, 509-534.
27. Leung, A. T., Imagawa, T., Block, B., Franzini-Armstrong, C. & Campbell, K. P. (1988). Biochemical and ultrastructural characterization of the 1,4-dihydropyridine receptor from rabbit skeletal-muscle-evidence for a 52,000 Da subunit. J. Biol. Chem. 263, 994-1001.
28. van Heel, M., Gowen, B., Matadeen, R., Orlova, E. V., Finn, R., Pape, T. et al. (2000). Single-particle electron cryo-microscopy: towards atomic resolution. Quart. Rev. Biophys. 33, 307-369.
29. Radermacher, M. (1988). 3-Dimensional reconstruction of single particles from random and nonrandom tilt series. J. Electron Microsc. Tech. 9, 359-394.
30. Schatz, M., Orlova, E. V., Dube, P., Jager, J. & van Heel, M. (1995). Structure of lumbricus-terrestris hemoglobin at 30 Å resolution determined using angular reconstitution. J. Struct. Biol. 114, 28-40.
31. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y. H., Ladjadj, M. & Leith, J. (1996). SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199.
32. Radermacher, M., Rao, V., Grassucci, R., Frank, J., Timerman, A. P., Fleischer, S. & Wagenknecht, T. (1994). Cryoelectron microscopy and 3-dimensional reconstruction of the calcium-release channel ryanodine receptor from skeletal-muscle. J. Cell Biol. 127, 411-423.
33. Saibil, H. (2000). Molecular chaperones: containers and surfaces for folding, stabilising or unfolding. Curr. Opin. Struct. Biol. 10, 251-258.
34. Chiu, W. & Schmid, M. F. (1997). Pushing back the limits of electron cryomicroscopy. Nature Struct. Biol. 4, 331-333.
35. Murata, K., Odahara, N., Kuniyasu, A., Sato, Y., Nakayama, H. & Nagayama, K. (2001). Asymmetric arrangement of auxiliary subunits of skeletal muscle voltage-gated L-type Ca2+ channel. Biochem. Biophys. Res. Commun. 282, 284-291.
36. Harris, J. R. & Horne, R. W. (1994). Negative staining: a brief assessment of current technical benefits, limitations and future possibilities. Micron, 25, 5-13.
37. Holzenburg, A., Flint, T. D., Shepherd, F. H. & Ford, R. C. (1996). Photosystem II: mapping the locations of the oxygen evolution-enhancing subunits by electron microscopy. Micron, 27, 121-127.
38. Rosenberg, M. F., Velarde, G., Ford, R. C., Martin, C., Berridge, G., Kerr, I. D. et al. (2001). Repacking of the transmembrane domains of P-glycoprotein during the transport ATPase cycle. EMBO J. 20, 5615-5625.
39. Berrow, N., Tedder, I., Page, K., Brice, N., Amos, B. & Dolphin, A. C. (1995). Properties of alpha(1a) calcium-channel currents is expressed in the Cos-7 cell-line. J. Physiol. (Lond.), 489P, P52-P53.
40. Flockerzi, V., Oeken, H.-J. & Hofmann, F. (1986). Purification of a functional receptor for calcium-channel blockers from rabbit skeletal-muscle microsomes. Eur. J. Biochem. 161, 217-224.
41. Tischendorf, G. W., Zeichhardt, H. & Stöffler, G. (1974). Determination of the location of proteins L14, L17, L18, L19, L22, and L23 on the surface of the 50 S ribosomal subunit of Escherichia coli by immunoelectron microscopy. Mol. Gen. Genet. 134, 187-204.
42. Venien-Bryan, C., Lowe, E. M., Boisset, N., Traxler, K. W., Johnson, L. N. & Carlson, G. M. (2002). Three-dimensional structure of phosphorylase kinase at 22 Å resolution and its complex with glycogen phosphorylase b. Structure, 10, 33-41.
43. Mayanagi, K., Miyata, T., Oyama, T., Ishino, T. & Morikawa, K. (2001). Three-dimensional electron microscopy of the clamp loader small subunit from Pyrococcus furiosus. J. Struct. Biol. 134, 35-45.
44. Penczek, P., Radermacher, M. & Frank, J. (1992). Three-dimensional reconstruction of single particles embedded in ice. Ultramicroscopy, 40, 33-53.
45. Frank, J. (1982). New methods for averaging non-periodic objects and distorted crystals in biologic electron microscopy. Optik, 63, 67-89.
46. Boekema, E. J. (1991). Negative staining of integral membrane proteins. Micron Microsc. Acta, 22, 361-369.
47. Böttcher, B., Wynne, S. A. & Crowther, R. A. (1997). Determination of the fold of the core protein of hepatitis B virus by electron microscopy. Nature, 386, 88-91.
48. Frank, J., Verschoor, A. & Boublik, M. (1981). Computer averaging of electron micrographs of 40 S ribosomal subunits. Science, 214, 1353-1355.
49. Sokolova, O., Kolmakova-Partensky, L. & Grigorieff, N. (2001). Three-dimensional structure of a voltage-gated potassium channel at 2.5 nm resolution. Structure, 9, 215-220.
50. Sato, C., Ueno, Y., Asai, K., Takahashi, K., Sato, M., Engel, A. & Fujiyoshi, Y. (2001). The voltage-sensitive sodium channel is a bell-shaped molecule with several cavities. Nature, 409, 1047-1051.
51. Lapie, P., Lory, P. & Fontaine, B. (1997). Hypokalemic periodic paralysis: an autosomal dominant muscle disorder caused by mutations in a voltage-gated calcium channel. Neuromusc. Disord. 7, 234-240.
52. Zühlke, R. D., Pitt, G. S., Deisseroth, K., Tsien, R. W. & Reuter, H. (1999). Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature, 399, 159-162.
53. Serysheva, I. I., Orlova, E. V., Chiu, W., Sherman, M. B., Hamilton, S. L. & van Heel, M. (1995). Electron cryomicroscopy and angular reconstitution used to visualize the skeletal-muscle calcium-release channel. Struct. Biol. 2, 18-24.
54. Samsó, M., Trujillo, R., Gurrola, G. B., Valdivia, H. H. & Wagenknecht, T. (1999). Three-dimensional location of the imperatoxin A binding site on the ryanodine receptor. J. Cell Biol. 146, 493-499.
55. Glossman, H. & Ferry, D. R. (1983). Solubilization and partial-purification of putative calcium channels labeled with nimodipine-H-3. Naunyn-Schmiedebergs Arch. Pharmacol. 323, 279-291.
56. Holzenberg, A., Shepherd, F. H. & Ford, R. C. (1994). Localization of the oxygen-evolving complex of photosystem-II by Fourier difference analysis. Micron, 25, 447-451.
57. Harris, J. R., Hoeger, U. & Adrian, M. (2001). Transmission electron microscopical studies on some haemolymph proteins from the marine polychaete Nereis virens. Micron, 32, 599-613.
58. Crowther, R. A., Henderson, R. & Smith, J. M. (1996). MRC image processing programs. J. Struct. Biol. 116, 9-16.
59. vanHeel, M. (1987). Similarity measures between images. Ultramicroscopy, 21, 95-99.
60. Harauz, G. & van Heel, M. (1986). Exact filters for general geometry three-dimensional reconstruction. Optik, 73, 146-156.
61. Holzenburg, A., Bewley, M. C., Wilson, F. H., Nicholson, W. V. & Ford, R. C. (1993). Three dimensional structure of photosystem II. Nature, 363, 470-472.