The portal protein of bacteriophage SPP1: a DNA pump with 13-fold symmetry (original) (raw)
Abstract
Electron microscopy in combination with image processing is a powerful method for obtaining structural information on non-crystallized biological macromolecules at the 10-50 A resolution level. The processing of noisy microscopical images requires advanced data processing methodologies in which one must carefully avoid the introduction of any form of bias into the data set. Using a novel multivariate statistical approach to the analysis of symmetry, we studied the structure of the bacteriophage SPP1 portal protein oligomer. This portal structure, ubiquitous in icosahedral bacteriophages which package dsDNA, is located at the site of symmetry mismatch between a 5-fold vertex of the icosahedral shell and the 6-fold symmetric (helical) tail. From previous studies such 'head-to-tail connector' structures were generally accepted to be homododecamers assembled in a 12-fold symmetric ring around a central channel. Using a new analysis methodology we have found that the phage SPP1 portal structure exhibits 13-fold cyclical symmetry: a new point group organization for oligomeric proteins. A model for the DNA packaging mechanism by 13-fold symmetric portal protein assemblies is presented which attributes a coherent functional meaning to their unusual symmetry.
Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bazinet C., Benbasat J., King J., Carazo J. M., Carrascosa J. L. Purification and organization of the gene 1 portal protein required for phage P22 DNA packaging. Biochemistry. 1988 Mar 22;27(6):1849–1856. doi: 10.1021/bi00406a009. [DOI] [PubMed] [Google Scholar]
- Bazinet C., King J. The DNA translocating vertex of dsDNA bacteriophage. Annu Rev Microbiol. 1985;39:109–129. doi: 10.1146/annurev.mi.39.100185.000545. [DOI] [PubMed] [Google Scholar]
- Boekema E. J., Berden J. A., van Heel M. G. Structure of mitochondrial F1-ATPase studied by electron microscopy and image processing. Biochim Biophys Acta. 1986 Oct 8;851(3):353–360. doi: 10.1016/0005-2728(86)90071-x. [DOI] [PubMed] [Google Scholar]
- Carazo J. M., Donate L. E., Herranz L., Secilla J. P., Carrascosa J. L. Three-dimensional reconstruction of the connector of bacteriophage phi 29 at 1.8 nm resolution. J Mol Biol. 1986 Dec 20;192(4):853–867. doi: 10.1016/0022-2836(86)90033-1. [DOI] [PubMed] [Google Scholar]
- Carrascosa J. L., Viñuela E., García N., Santisteban A. Structure of the head-tail connector of bacteriophage phi 29. J Mol Biol. 1982 Jan 15;154(2):311–324. doi: 10.1016/0022-2836(82)90066-3. [DOI] [PubMed] [Google Scholar]
- Crowther R. A., Amos L. A. Harmonic analysis of electron microscope images with rotational symmetry. J Mol Biol. 1971 Aug 28;60(1):123–130. doi: 10.1016/0022-2836(71)90452-9. [DOI] [PubMed] [Google Scholar]
- Donate L. E., Carrascosa J. L. Characterization of a versatile in vitro DNA-packaging system based on hybrid lambda/phi 29 proheads. Virology. 1991 Jun;182(2):534–544. doi: 10.1016/0042-6822(91)90594-2. [DOI] [PubMed] [Google Scholar]
- Donate L. E., Herranz L., Secilla J. P., Carazo J. M., Fujisawa H., Carrascosa J. L. Bacteriophage T3 connector: three-dimensional structure and comparison with other viral head-tail connecting regions. J Mol Biol. 1988 May 5;201(1):91–100. doi: 10.1016/0022-2836(88)90441-x. [DOI] [PubMed] [Google Scholar]
- Donate L. E., Murialdo H., Carrascosa J. L. Production of lambda-phi 29 phage chimeras. Virology. 1990 Dec;179(2):936–940. doi: 10.1016/0042-6822(90)90172-n. [DOI] [PubMed] [Google Scholar]
- Driedonks R. A., Engel A., tenHeggeler B., van Driel Gene 20 product of bacteriophage T4 its purification and structure. J Mol Biol. 1981 Nov 15;152(4):641–662. doi: 10.1016/0022-2836(81)90121-2. [DOI] [PubMed] [Google Scholar]
- Guo P., Peterson C., Anderson D. Prohead and DNA-gp3-dependent ATPase activity of the DNA packaging protein gp16 of bacteriophage phi 29. J Mol Biol. 1987 Sep 20;197(2):229–236. doi: 10.1016/0022-2836(87)90121-5. [DOI] [PubMed] [Google Scholar]
- Henderson R., Baldwin J. M., Ceska T. A., Zemlin F., Beckmann E., Downing K. H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol. 1990 Jun 20;213(4):899–929. doi: 10.1016/S0022-2836(05)80271-2. [DOI] [PubMed] [Google Scholar]
- Hendrix R. W. Symmetry mismatch and DNA packaging in large bacteriophages. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4779–4783. doi: 10.1073/pnas.75.10.4779. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jiménez J., Santisteban A., Carazo J. M., Carrascosa J. L. Computer graphic display method for visualizing three-dimensional biological structures. Science. 1986 May 30;232(4754):1113–1115. doi: 10.1126/science.3754654. [DOI] [PubMed] [Google Scholar]
- Kochan J., Carrascosa J. L., Murialdo H. Bacteriophage lambda preconnectors. Purification and structure. J Mol Biol. 1984 Apr 15;174(3):433–447. doi: 10.1016/0022-2836(84)90330-9. [DOI] [PubMed] [Google Scholar]
- Sass H. J., Büldt G., Beckmann E., Zemlin F., van Heel M., Zeitler E., Rosenbusch J. P., Dorset D. L., Massalski A. Densely packed beta-structure at the protein-lipid interface of porin is revealed by high-resolution cryo-electron microscopy. J Mol Biol. 1989 Sep 5;209(1):171–175. doi: 10.1016/0022-2836(89)90180-0. [DOI] [PubMed] [Google Scholar]
- Schatz M., van Heel M. Invariant classification of molecular views in electron micrographs. Ultramicroscopy. 1990 Mar-Apr;32(3):255–264. doi: 10.1016/0304-3991(90)90003-5. [DOI] [PubMed] [Google Scholar]
- Tavares P., Santos M. A., Lurz R., Morelli G., de Lencastre H., Trautner T. A. Identification of a gene in Bacillus subtilis bacteriophage SPP1 determining the amount of packaged DNA. J Mol Biol. 1992 May 5;225(1):81–92. doi: 10.1016/0022-2836(92)91027-m. [DOI] [PubMed] [Google Scholar]
- van Heel M., Frank J. Use of multivariate statistics in analysing the images of biological macromolecules. Ultramicroscopy. 1981;6(2):187–194. doi: 10.1016/0304-3991(81)90059-0. [DOI] [PubMed] [Google Scholar]
- van Heel M. Multivariate statistical classification of noisy images (randomly oriented biological macromolecules). Ultramicroscopy. 1984;13(1-2):165–183. doi: 10.1016/0304-3991(84)90066-4. [DOI] [PubMed] [Google Scholar]
- van Heel M., Stöffler-Meilicke M. Characteristic views of E. coli and B. stearothermophilus 30S ribosomal subunits in the electron microscope. EMBO J. 1985 Sep;4(9):2389–2395. doi: 10.1002/j.1460-2075.1985.tb03944.x. [DOI] [PMC free article] [PubMed] [Google Scholar]