Structure of keyhole limpet hemocyanin type 1 (KLH1) at 15 Å resolution by electron cryomicroscopy and angular reconstitution

Journal of Molecular Biology

Volumn 271, Issue 3, 1997, Pages 417-437

  Orlova, Elena V ^a,b   Dube, Prakash ^a,c   Harris, J Robin ^d   Beckman, Erich ^b   Zemlin, Friedrich ^b   Markl, Jürgen ^d   Van Heel, Marin ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b FRITZ HABER INSTITUT DER MAX PLANCK GESELLSCHAFT   (Germany)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Angular reconstitution; Electron cryomicroscopy; High contrast embedding; Keyhole limpet hemocyanin; Single particle analysis

Indexed keywords

GLUCOSE; HELIUM; IMMUNOSTIMULATING AGENT; KEYHOLE LIMPET HEMOCYANIN; MOLYBDIC ACID; OLIGOMER;

ARTICLE; DRUG STRUCTURE; ELECTRON MICROSCOPY; IMAGE PROCESSING; LOW TEMPERATURE PROCEDURES; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN QUATERNARY STRUCTURE;

CEPHALOPODA;

EID: 0031583477     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1182     Document Type: Article

References (94)

1. Akey C. W., Edelstein C. J. Equivalence of the projected structure of thin catalase crystals preserved for electron microscopy by negative stain, glucose, or embedding in the presence of tannic acid. J. Mol. Biol. 163:1983;575-612.
2. Billiald P., Lamy J., Wichertjes T., van Bruggen E. F. J., Loncke P., Gielens C., Préaux G. Immunoelectron microscopy of the hemocyanins ofOctopus dofleiniOctopus vulgaris. Invertebrate Dioxygen Carriers. 1990;Leuven University Press, Louvain.
3. Boettcher C., Stark H., van Heel M. Stacked bilayer helices: a new structural organization of amphiphilic molecules. Ultramicroscopy. 62:1996;133-139.
4. Borland L., van Heel M. Classification of image data in conjugate representation spaces. J. Optic. Soc. Am. ser. A. 7:1990;601-610.
5. Böttcher. Determination of the fold of the core protein of hepatitis B virus by electron microscopy. Nature. 385:1997;88-91.
6. Bracewell R. N. Strip integration in radio astronomy. Aust. J. Phys. 9:1956;198-217.
7. Bracewell R. N. Two-dimensional aerial smoothing in radio astronomy. Aust. J. Phys. 9:1960;297-314.
8. Bremer A., Henn C., Engel A., Baumeister W., Aebi A. Has negative staining still a place in biomolecular electron microscopy? Ultramicroscopy. 46:1992;85-111.
9. Brenner S., Horne R. W. A negative staining method for high resolution electron microscopy of viruses. Biochim. Biophys. Acta. 34:1959;103-110.
10. Cejka Z., Santini C., Tognon G., Ghiretti Magaldi A. The molecular architecture of the extracellular hemoglobin ofOphelia bicornis. J. Struct. Biol. 107:1991;259-267.
11. Cejka Z., Kleinz J., Santini C., Hegerl R., Ghiretti Magaldi A. The molecular architecture of the extracellular hemoglobin ofOphelia bicornis. J. Struct. Biol. 109:1992;52-60.
12. Conway. Visualization of a 4-helix bundle in the hepatitis B virus capsid by cryo-electron microscopy. Nature. 385:1997;91-94.
13. Crowther R. A., DeRosier D. J., Klug A. The reconstruction of a three-dimensional structure from projections and its application to electron microscopy. Proc. Roy. Soc. London. 317:1970a;319-340.
14. Crowther R. A., Amos L. A., Finch J. T., DeRosier D. J., Klug A. Three dimensional reconstruction of spherical viruses by Fourier synthesis from electron micrographs. Nature. 226:1970b;421-425.
15. DeRosier D. J., Klug A. Reconstruction of three-dimensional structures from electron micrographs. Nature. 217:1968;130-134.
16. DeRosier D. J., Moore P. B. Reconstruction of three-dimensional images from electron micrographs of structures with helical symmetry. J. Mol. Biol. 52:1970;355-369.
17. Dube P., Orlova E. V., Zemlin F., van Heel M., Harris J. R., Markl J. Three-dimensional structure of keyhole limpet hemocyanin by cryoelectron microscopy and angular reconstitution. J. Struct. Biol. 115:1995a;226-232.
18. Dube P., Stark H., Orlova E. V., Schatz M., Beckmann E., Zemlin F., van Heel M. 3D structure of single macromolecules at 15 Å resolution by cryomicroscopy and angular reconstitution. Bailey G. W., Ellisman M. H., Henningar R. A., Zaluzec N. J. Proceedings of Microscopy and Microanalysis. 1995b;Jones and Begell Publ, New York.
19. Dubochet J., Adrian M., Chang J.-J., Homo J.-C., Lepault J., McDowall A., Schultz P. Cryo-electron microscopy of vitrified specimens. Quart. Rev. Biophys. 21:1988;129-228.
20. Frank J., Verschoor A., Boublik M. Computer averaging of electron micrographs of 40S ribosomal subunits. Science. 214:1981;1353-1355.
21. Frank J., Penczek P., Grassucci R., Srivastava S. Three-dimensional reconstruction of the 70 SEscherichia coli. J. Cell Biol. 115:1991;597-605.
22. Fernandez-Morán H., van Bruggen E. F: J., Ohtsuki M. Macromolecular organization of hemocyanins and apohemocyanins as revealed by electron microscopy. J. Mol. Biol. 16:1966;191-207.
23. Gebauer W., Harris J. R., Heid H., Süling M., Hillenbrand R., Söhngen S., Wegener-Strake A., Markl J. Quaternary structure, subunits and domain patterns of two discrete forms of keyhole limpet hemocyanin: KLH1 and KLH2. Zoology. 98:1994;51-68.
24. Goncharov A. B., Gelfand M. S. Determination of mutual orientation of identical particles from their projections by the moments method. Ultramicroscopy. 25:1988;317-328.
25. Harauz G., van Heel M. Exact filters for general geometry three-dimensional reconstruction. Optik. 73:1986;146-156.
26. Harris J. R., Horne R. W. Negative staining: a brief assessment of current technical benefits, limitations and future possibilities. Micron. 25:1994;5-13.
27. Harris J. R., Cejka Z., Wegener-Strake A., Gebauer W., Markl J. Two-dimensional crystallization, transmission electron microscopy and image processing of keyhole limpet hemocyanin. Micron Microsc. Acta. 23:1992;287-301.
28. Harris J. R., Gebauer W., Markl J. Immunoelectron microscopy of hemocyanin from the keyhole limpet (Megathura crenulata. J. Struct. Biol. 111:1993;96-104.
29. Harris J. R., Gebauer W., Söhngen S. M., Markl J. Keyhole limpet hemocyanin (KLH): purification of intact KLH1 through selective dissociation of KLH2. Micron. 26:1995a;201-212.
30. Harris J. R., Gebauer W., Markl J. Keyhole limpet haemocyanin: negative staining in the presence of trehalose. Micron. 26:1995b;25-33.
31. Harris J. R., Gebauer W., Söhngen S. M., Nermut M. V., Markl J. Keyhole limpet hemocyanin (KLH)II: Characteristic reassociation properties of purified KLH1 and KLH2. Micron. 28:1997;43-56.
32. Hawkes P. W. Image processing based on linear theory of image formation. Hawkes P. W. Computer Processing of Electron Microscope Images. 1980;Springer Verlag, Berlin, Heidelberg and New York.
33. D3. Cancer Res. 54:1994;197-203.
34. Henderson R. The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules. Quart. Rev. Biophys. 28:1995;171-193.
35. Henderson R., Unwin P. N. T. Three-dimensional model of purple membrane obtained by electron microscopy. Nature. 257:1975;28-32.
36. Henderson R., Baldwin J. M., Ceska T. A., Zemlin F., Beckman E., Downing K. H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryomicroscopy. J. Mol. Biol. 213:1990;899-929.
37. Jap B. K., Walian P. J. Biophysics of the structure and function of porins. Quart. Rev. Biophys. 23:1990;367-403.
38. Kellenberger E., Haener M., Wurtz M. The wrapping phenomenon in air-dried and negatively stained preparations. Ultramicroscopy. 9:1982;139-150.
39. Kühlbrandt W., Wang D. N. Three-dimensional structure of plant light-harvesting complex determined by electron crystallography. Nature. 350:1991;130-134.
40. vb. J. Mol. Biol. 238:1994;75-87.
41. Lambert O., Taveau J.-C., Boisset N., Lamy J. N. Three-dimensional reconstruction of the hemocyanin of the protobranch bivalve molluscNucula hanleyi. Arch. Biochem. Biophys. 319:1995a;231-243.
42. DcHelix pomatia. J. Mol. Biol. 248:1995b;431-448.
43. Lamy J., Gielens C., Lambert O., Taveau J.-C., Motta G., Lonche P., De Geest N., Preaux G., Lamy J. Further approaches to the quaternary structure ofOctopus. Arch. Biochem. Biophys. 305:1993;17-29.
44. Lefranc G., Knapek K., Dietrich I. Superconducting lens design. Ultramicroscopy. 10:1982;111-124.
45. Longenecker B. M., Reddish M., Koganty R., MacLean G. D. Immune responses of mice and human breast cancer patients following immunization with synthetic sialyl-Tn conjugated to KLH plus DETOX adjuvant. Ann. New York Acad. Sci. 690:1993;276-291.
46. Malecki M., Ris H. Deep negative staining of cell whole mounts for high voltage electron microscopy. Bailey G. W., Rieder C. L. Proceedings of the 51st Annual Meeting of the Microscopical Society of America Cincinnati. 1993;San Francisco Press, San Francisco.
47. Markl J., Decker H. Molecular structure of the arthropod hemocyanins. Advances in Comparative and Environmental Physiology. 1992;Springer-Verlag, Berlin and Heidelberg.
48. Markl J., Savel-Niemann A., Wegener-Strake A., Süling A., Schneider A., Gebauer W., Harris J. R. The role of two distinct subunit types in the architecture of keyhole limpet hemocyanin (KLH). Naturwissenschaften. 78:1991;512-514.
49. Mellema J. E., Klug A. Quaternary structure of gastropod haemocyanin. Nature. 229:1972;146-150.
50. Miller K. I., Schabtach E., van Holde K: E. Arrangement of subunits and domains within theOctopus dofleini. Proc. Natl Acad. Sci. USA. 87:1990;1496-1500.
51. Naylor P. H., Sztein M. B., Wada S., Maurer S., Holterman D., Kirkley J. E., Naylor C. W., Zook B. C., Hitzelberg R. A., Gibbs C. J. Jr. Preclinical and clinical studies on immunogenicity and safety of the HIV-1 p17-based synthetic peptide AIDS vaccine- HPG-30-KLH. Int. J. Immunopharmacol. 13 (Suppl. 1):1991;117-127.
52. Orlova E. V., van Heel M. Angular reconstitution of macromolecules with arbitrary point-group symmetry. Jouffrey B., Colliex C. Proceedings of the 13th International Congress on Electron Microscopy. 1994;Les Editions de Physique, Les Ulis.
53. Orlova E. V., Serysheva I. I., van Heel M., Hamilton S. L., Chiu W. Two structural configurations of the skeletal muscle calcium release channel. Nature Struct. Biol. 3:1996a;547-552.
54. Orlova E. V., Dube P., Harris J. R., Beckman E., Zemlin F., Schatz M., Markl J., van Heel M. Three-dimensional structure of keyhole limpet hemocyanin type 1 (KLH1) at 15 Å CD Proceedings of the 11th European Congress of Electron Microscopy. 1996b;European Microscopical Society (EMS), Dublin.
55. Penczek P., Grassucci R. A., Frank J. The ribosome at improved resolution: new techniques for merging and orientation refinements in 3D cryo-electron microscopy of biological particles. Ultramicroscopy. 53:1994;251-270.
56. Radermacher M. Three-dimensional reconstruction of single particles from random and nonrandom tilt series. J. Elect. Microsc. Tech. 9:1988;359-394.
57. Radermacher M. Three-dimensional reconstruction from random projections: orientational alignment via radon transforms. Ultramicroscopy. 53:1994;121-136.
58. Ris H., Allen C. Embedding in negative stain as a method to preserve and contrast isolated cell organelles for high voltage electron microscopy. Fourth International Conference on High Voltage Electron Microscopy, Toulouse. 1975.
59. Saxton W. O., Baumeister W. The correlation averaging of a regularly arranged bacterial cell envelope protein. J. Microsc. 127:1982;127-138.
60. Schatz M., Orlova E. V., Dube P., Jäger J., van Heel M. Structure ofLumbricus terrestris. J. Struct. Biol. 114:1995;28-44.
61. Serysheva I., Orlova E. V., Sherman M., Chiu W., Hamilton S., van Heel M. The skeletal muscle calcium-release channel in its closed state visualized by electron cryomicroscopy and angular reconstitution. Nature Struct. Biol. 2:1995;14-18.
62. Sherman M. B., Orlova E. V., Terzyan S. S., Kleine R., Kiselev N. A. On the negative staining of the protein crystal structure. Ultramicroscopy. 7:1981;131-138.
63. Siezen R. J., van Bruggen E. F. J. Structure and properties of hemocyanins XII. Electron microscopy of dissociation products ofHelix pomatia. J. Mol. Biol. 90:1974;77-89.
64. Söhngen S. M., Stahlmann A., Markl J. On the domain structure of KLH, the hemocyanin from the gastropodMegathura crenulata. Verh. Dsch. Zool. Ges. 88:1995;135.
65. Söhngen S. M., Stahlmann A., Harris J. R., Mueller S. A., Engel A., Markl J. Mass determination, subunit organization, and control of oligomerization states of keyhole limpet hemocyanin. Eur. J. Biochem. in the press:1997.
66. Stanley W., Anderson T. Electron micrographs of protein structures. J. Biol. Chem. 146:1942;24-33.
67. Stark H., Mueller F., Orlova E. V., Schatz M., Dube P., Erdemir T., Zemlin F., Brimacombe R., van Heel M. The 70S ribosome at 23 Å resolution: fitting the ribosomal RNA. Structure. 3:1995;815-821.
68. Stark H., Orlova E. V., Rinke-Appel J., Jünke N., Mueller F., Schatz, Rodnina M., Wintermeyer W., Brimacombe R., van Heel M. Arrangement of tRNAs in pre- and post-translocational ribosomes revealed by electron cryomicroscopy. Cell. 88:1997;19-28.
69. Stoops J. K., Baker T. S., Schroeter J. P., Kolodziej S. J., Niu X. D., Reed L. J. Three-dimensional structure of the truncated core of theSaccharomyces cerevisiae. J. Biol. Chem. 267:1992;24769-24775.
70. Swerdlow R. D., Ebert R. F., Lee P., Bonaventura C., Miller K. I. Keyhole limpet hemocyanin: structural and functional characterization of two different subunits and multimers. Comp. Biochem. Physiol. 113B:1996;537-548.
71. Tavares P., Droege A., Lurz R., Gräber I., Orlova E. V., Dube P., Van Heel M. The SPP1 Connection. FEMS Microb. Rev. 17:1995;47-56.
72. Unwin P. N. T., Henderson R. Molecular structure determination by electron microscopy of unstained crystalline specimens. J. Mol. Biol. 94:1975;425-440.
73. Unwin P. T. N., Klug A. Electron microscopy of the stacked disk aggregate of tobacco mosaic virus protein I. Three-dimensional image reconstruction. J. Mol. Biol. 87:1974;641-656.
74. van Breemen J. F. L., Wichertjes T., Muller M. F. J., van Driel R., van Bruggen E. F. J. Tubular polymers derived fromHelix pomatia. Eur. J. Biochem. 100:1975;61-65.
75. van Breemen J. F. L., Ploegman J. H., van Bruggen E. F. J. Structure ofHelix pomatia. Eur. J. Biochem. 100:1979;61-65.
76. van Bruggen E. F. J. Electron microscopy of hemocyanins 1942-1986. Micron Microsc. Acta. 2:1986;167-173.
77. van Bruggen E. F: J., Wiebenga E. H., Gruber M. Negative-staining electron microscopy of proteins at pH values below their isoelectric points. Its application to hemocyanin. Biochim. Biophys. Acta. 42:1960;171-172.
78. van Heel M. Multivariate statistical classification of noisy images (randomly orientated biological macromolecules). Ultramicroscopy. 7:1984;165-183.
79. van Heel M. Similarity measures between images. Ultramicroscopy. 21:1987a;95-100.
80. van Heel M. Angular reconstitution:a posteriori. Ultramicroscopy. 21:1987b;111-124.
81. van Heel M. Classification of very large electron microscopical data sets. Optik. 82:1989;114-126.
82. van Heel M. Fast transposing of large multi-dimensional image data sets. Ultramicroscopy. 38:1991;75-84.
83. van Heel M., Dube P. Quaternary structure of multi-hexameric arthropod hemocyanins. Micron. 25:1994;387-418.
84. van Heel M., Frank J. Use of multivariate statistics in analyzing the images of biological macromolecules. Ultramicroscopy. 6:1981;187-194.
85. van Heel M., Harauz G. Resolution criteria for three dimensional reconstructions. Optik. 73:1986;119-122.
86. van Heel M., Keegstra W. IMAGIC: a fast, flexible and friendly image analysis software system. Ultramicroscopy. 7:1981;113-130.
87. van Heel M., Stöffler-Meilicke M. Characteristic views ofE. coliB. stearothermophilus. EMBO J. 4:1985;2389-2395.
88. van Heel M., Schatz M., Orlova E. Correlation functions revisited. Ultramicroscopy. 46:1992a;307-316.
89. van Heel M., Winkler H.-P., Orlova E. V., Schatz M. Structural analysis of ice-embedded single particles. Scanning Microsc. (Suppl). 6:1992b;23-42.
90. van Heel M., Harauz G., Orlova E. V., Schmidt R., Schatz M. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116:1996;17-24.
91. van Holde K. E., Miller K. I. Hemocyanins. Anfinsen C. B., Edsall J. T., Eisenberg D. S., Richards F. M. Advances in Protein Chemistry. 1995;Academic Press Inc, New York.
92. Wishahi M. M., Ismail I. M., Ruebben H., Otto T. Keyhole-limpet hemocyanin immunotherapy in the bilharzial bladder: a new treatment modality? Phase II trial: superficial bladder cancer. J. Urol. 153:1995;926-928.
93. Yacyshyn M. B. B., Poppema S., Berg A., Maclean G. D., Reddish M. A., Meikle A., Longenecker B. M. Activation antigens on peripheral-blood lymphocyte populations in metastatic breast and ovarian cancer patients-correlations with survival following active specific immunotherapy. Int. J. Cancer. 61:1995;470-474.
94. Zemlin F., Beckmann E., van der Mast K. D. A 200 kV electron microscope with Schottky field emitter and a helium-cooled superconducting objective lens. Ultramicroscopy. 63:1996;227-238.