Structure of frozen-hydrated triad junctions: A case study in motif searching inside tomograms

Journal of Structural Biology

Volumn 165, Issue 2, 2009, Pages 53-63

  Renken, Christian ^a   Hsieh, Chyong ere ^a   Marko, Michael ^a   Rath, Bimal ^a   Leith, Ardean ^a   Wagenknecht, Terry ^a   Frank, Joachim ^a,b   Mannella, Carmen A ^a  

^a WADSWORTH CENTER   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Calsequestrin; Cryo electron tomography; Ryanodine receptor; Skeletal muscle; Template matching; Triad junctions

Indexed keywords

CALSEQUESTRIN; RYANODINE RECEPTOR;

ARTICLE; CALCIUM TRANSPORT; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; SARCOPLASMIC RETICULUM; TOMOGRAPHY;

ANIMALS; CALCIUM; CALSEQUESTRIN; CRYOELECTRON MICROSCOPY; CYTOPLASM; IMAGE PROCESSING, COMPUTER-ASSISTED; INTERCELLULAR JUNCTIONS; MODELS, BIOLOGICAL; MULTIVARIATE ANALYSIS; MUSCLE, SKELETAL; RABBITS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; SOFTWARE; TOMOGRAPHY;

EID: 58349106468     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2008.09.011     Document Type: Article

References (43)

1. Anderson A.A., Treves S., Biral D., Betto R., Sandona D., Ronjat M., and Zorzato F. The novel skeletal muscle sarcoplasmic reticulum JP-45 protein: molecular cloning, tissue distribution, developmental expression, and interaction with α1.1 subunit of the voltage-gated calcium channel. J. Biol. Chem. 278 (2003) 39987-39992
2. Beck M., Foerster F., Ecke M., Plitzko J., Melchior F., Gerisch G., Baumeister W., and Ohad M. Nuclear pore complex structure and dynamics revealed by cryoelectron tomography. Science 306 (2004) 1387-1390
3. Boehm J., Frangakis A.S., Hergerl R., Nickell S., Typke D., and Baumeister W. Toward detecting and identifying macromolecules in a cellular context: template matching applied to electron tomograms. Proc. Natl. Acad. Sci. USA 97 (2000) 14245-14250
4. Bonetta L. Zooming in on electron tomography. Nat. Methods 2 (2005) 139-144
5. Brandt N.R., Caswell A.H., Wen S.R., and Talvenheimo J.A. Molecular interactions of the junctional foot protein and dihydropyridine receptor in skeletal muscle triads. J. Membrane Biol. 113 (1990) 237-251
6. Chou T., Kim K.S., and Oster G. Statistical thermodynamics of membrane bending-mediated protein-protein attractions. Biophys. J. 80 (2001) 1075-1087
7. Crowther R.A., DeRosier D.J., and Klug A. The reconstruction of a three dimensional structure from projections and its application to electron microscopy. Proc. Roy. Soc. Lond. A 317 (1970) 319-340
8. Dan N., and Safran S.A. Effect of lipid characteristics on the structure of transmembrane proteins. Biophys. J. 75 (1998) 1410-1414
9. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., and Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 (1996) 190-199
10. Frank J., Wagenknecht T., McEwen B.F., Marko M., Hsieh C., and Mannella C.A. Three-dimensional imaging of biological complexity. J. Struct. Biol. 138 (2002) 85-91
11. Frankgakis A., Boehm J., Foerster F., Nickell S., Nicastro D., Typke D., Hegerl R., and Baumeister W. Identification of macromolecular complexes in cryoelectron tomograms of phantom cells. Proc. Natl. Acad. Sci. USA 99 (2002) 14153-14158
12. Franzini-Armstrong C., Kenney L.J., and Varriano-Marston E. The structure of calsequestrin in triads of vertebrate skeletal muscle: a deep-etch study. J. Cell Biol. 105 (1987) 49-56
13. 2+ release units and couplons in skeletal and cardiac muscles. Biophys. J. 77 (1999) 1528-1539
14. Hsieh C.E., Leith A., Mannella C.A., Frank J., and Marko M. Towards high-resolution three-dimensional imaging of native mammalian tissue: electron tomography of frozen-hydrated rat liver sections. J. Struct. Biol. 153 (2006) 1-13
15. Hsieh C.E., Marko M., Frank J., and Mannella C.A. Electron tomographic analysis of frozen-hydrated tissue sections. J. Struct. Biol. 138 (2002) 63-73
16. Jones L.R., Zhang L., Sanborn K., Jorgensen A.O., and Kelley J. Purification, primary structure, and immunological characterization of the 26-kDa calsequestrin binding protein (junctin) from cardiac junctional sarcoplasmic reticulum. J. Biol. Chem. 270 (1995) 30787-30796
17. Lewis, J.P., 1995. Fast template matching. In: Vision Interface 120-123 Proceedings of the Canadian Image Processing and Pattern Recognition Society, Quebec City, Quebec, Canada, May 15-19, 1995.
18. Marko M., Hsieh C.-B., Schalek R., Frank J., and Mannella C.A. Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy. Nat. Methods 4 (2007) 215-217
19. 2+ release channels (ryanodine receptors). Science 281 (1998) 818-821
20. Nicastro D., McIntosh J.R., and Baumeister W. 3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography. Proc. Natl. Acad. Sci. USA 102 (2005) 15889-15894
21. Ortiz J.O., Forster F., Kurner J., Linaroudis A., and Baumeister W. Mapping 70S ribosomes in intact cells by cryoelectron tomography and pattern recognition. J. Struct. Biol. 156 (2006) 334-341
22. Paolini C., Protasi F., and Franzini-Armstrong C. The relative position of RyR feet and DHPR tetrads in skeletal muscle. J. Molec. Biol. 342 (2004) 145-153
23. Penczek P., Marko M., Buttle K., and Frank J. Double-tilt electron tomography. Ultramicroscopy 60 (1995) 393-410
24. Radermacher M., Rao V., Grassucci R., Frank J., Timerman A.P., Fleischer S., and Wagenknecht T. Cryo-electron microscopy and three-dimensional reconstruction of the calcium release channel/ryanodine receptor from skeletal muscle. J. Cell Biol. 127 (1994) 411-423
25. Rath B.K., Marko M., Radermacher M., and Frank J. Low-dose automated electron tomography: a recent implementation. J. Struct. Biol. 120 (1997) 210-218
26. Rath B.K., Hergerl R., Leith A., Shaikh T.R., Wagenknecht T., and Frank J. Fast 3D motif search of EM density maps using a locally normalized cross-correlation function. J. Struct. Biol. 144 (2003) 95-103
27. Roseman A.M. Particle finding in electron micrographs using a fast local correlation. Ultramicroscopy 94 (2003) 225-236
28. Rossi A.M., and Dirksen R.T. Sarcoplasmic reticulum: the dynamic calcium governor of muscle. Muscle & Nerve 33 (2006) 715-731
29. Saito A., Seiler S., Chu A., and Fleischer S. Preparation and morphology of sarcoplasmic reticulum terminal cisternae from rabbit skeletal muscle. J. Cell Biol. 99 (1984) 875-885
30. Sali A., Glaeser R., Barnest T., and Baumeister W. From words to literature in structural proteomics. Nature 422 (2003) 216-225
31. Samso M., Wagenknecht T., and Allen P.D. Internal structure and visualization of transmembrane domains of the RyR1 calcium release channel by cryo-EM. Nat. Struct. Molec. Biol. 12 (2005) 539-544
32. 2+ release channel at 14 A resolution. J. Molec. Biol. 345 (2005) 427-431
33. Stern M.D., Song L.S., Cheng H.P., Sham J.S.K., Yang H.T., Boheler K.R., and Rios D.E. Local control models of cardiac excitation-contraction coupling-a possible role for allosteric interactions between ryanodine receptors. J. Gen. Physiol. 113 (1999) 469-489
34. Takeshima H., Komazaki S., Nishi M., Iino M., and Kangawa K. Junctophilins: a novel family of junctional membrane complex proteins. Mole. Cell 6 (2000) 11-22
35. Takeshima H., Shimuta M., Komazaki S., Ohmi K., Nishi M., Iino M., Miyata A., and Kangawa K. Mitsugumin29, a novel synaptophysin family member from the triad junction in skeletal muscle. Biochem. J. 331 (1998) 317-322
36. Treves S., Feriotto G., Moccagatta L., Gambari R., and Zorzato F. Molecular cloning, expression, functional characterization, chromosomal localization, and gene structure of junctate a novel integral calcium binding protein of sarco(endo)plasmic reticulum membrane. J. Biol. Chem. 275 (2000) 39555-39568
37. Wagenknecht T., Hsieh C.-E., Rath B.K., Fleischer S., and Marko M. Electron tomography of frozen-hydrated isolated triad junctions. Biophys. J. 83 (2002) 2491-2501
38. Wagenknecht T., Radermacher M., Grassucci R., Berkowitz J., Xin H.B., and Fleischer S. Locations of calmodulin and FK506-binding protein on the three-dimensional architecture of the skeletal muscle ryanodine receptor. J. Biol. Chem. 272 (1997) 32463-32471
39. 2+ release. J. Cell Biol. 174 (2006) 639-645
40. Wang S., Trumble W.R., Liao H., Wesson C.R., Dunker A.K., and Kang C.H. Crystal structure of calsequestrin from rabbit skeletal muscle sarcoplasmic reticulum. Nat. Struct. Biol. 5 (1998) 476-483
41. Yin C.C., and Lai F.A. Intrinsic lattice formation by the ryanodine receptor calcium-release channel. Nat. Cell Biol. 2 (2000) 669-671
42. Zalk R., Lehnart S.E., and Marks A.R. Modulation of the ryanodine receptor and intracellular calcium. Ann. Rev. Biochem. 76 (2007) 367-385
43. Zorzato F., Anderson A.A., Ohlendieck K., Froemming G., Guerrini R., and Treves S. Identification of a novel 45 kDa protein (JP-45) from rabbit sarcoplasmic-reticulum junctional-face membrane. Biochem. J. 351 (2000) 537-543