Identification of subunit-subunit interactions in bacteriophage P22 procapsids by chemical cross-linking and mass spectrometry

Journal of Proteome Research

Volumn 5, Issue 2, 2006, Pages 370-377

  Kang, Sebyung ^a   Hawkridge, Adam M ^c,d   Johnson, Kenneth L ^c   Muddiman, David C ^c,d   Prevelige Jr , Peter E ^b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c MAYO CLINIC   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Bacteriophage P22; Capsid interactions; Chemical cross linking; Mass spectrometry

Indexed keywords

COAT PROTEIN; CYSTEINE; DEUTERIUM; DOUBLE STRANDED DNA; HYDROGEN; LYSINE; PROTEIN SUBUNIT; THREONINE; VIRUS DNA;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIOPHAGE P22; CONTROLLED STUDY; CROSS LINKING; CRYSTAL STRUCTURE; DISULFIDE BOND; DNA PACKAGING; DNA VIRUS; MASS SPECTROMETRY; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; VIRUS CAPSID; VIRUS PROCAPSID;

AMINO ACID SUBSTITUTION; BACTERIOPHAGE P22; CAPSID; CAPSID PROTEINS; CROSS-LINKING REAGENTS; CYSTEINE; MASS SPECTROMETRY; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN SUBUNITS; THREONINE; VIRUS ASSEMBLY;

DNA VIRUSES; MIRIDAE;

EID: 32344436397     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr050356f     Document Type: Article

References (35)

1. Alberts, B. The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 1998, 92 (3), 291-294.
2. Caspar, D. Movement and self-control in protein assemblies. Quasi-equivalence revisited. Biophys. J. 1980, 32 (1), 103-138.
3. Crick, F. H. C.; Watson, J. D. Structure of small viruses. Nature 1956, 177 (4506), 473-475.
4. Wikoff, W. R.; Liljas, L.; Duda, R. L.; Tsuruta, H.; Hendrix, R. W.; Johnson, J. E. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 2000, 289 (5487), 2129-2133.
5. Jiang, W.; Li, Z.; Zhang, Z.; Baker, M. L.; Prevelige, P. E., Jr.; Chiu, W. Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat. Struct. Biol. 2003, 10 (2), 131-135.
6. Prasad, B. V.; Prevelige, P. E.; Marietta, E.; Chen, R. O.; Thomas, D.; King, J.; Chiu, W. Three-dimensional transformation of capsids associated with genome packaging in a bacterial virus. J. Mol. Biol. 1993, 231 (1), 65-74.
7. Kang, S.; Prevelige, P. E., Jr. Domain study of bacteriophage p22 coat protein and characterization of the capsid lattice transformation by hydrogen/deuterium exchange. J. Mol. Biol. 2005, 347 (5), 935-948.
8. Lanman, J.; Lam, T. T.; Barnes, S.; Sakalian, M.; Emmett, M. R.; Marshall, A. G.; Prevelige, P. E., Jr. Identification of novel interactions in HIV-1 capsid protein assembly by high-resolution mass spectrometry. J. Mol. Biol. 2003, 325 (4), 759-772.
9. Tuma, R.; Coward, L. U.; Kirk, M. C.; Barnes, S.; Prevelige, P. E., Jr. Hydrogen-deuterium exchange as a probe of folding and assembly in viral capsids. J. Mol. Biol. 2001, 306 (3), 389-396.
10. King, J.; Lenk, E. V.; Botstein, D. Mechanism of head assembly and DNA encapsulation in Salmonella phage P22. II. Morphogenetic pathway. J. Mol. Biol. 1973, 80 (4), 697-731.
11. King, J.; Casjens, S. Catalytic head assembling protein in virus morphogenesis. Nature 1974, 251 (5471), 112-119.
12. Casjens, S.; King, J. P22 morphogenesis. I: Catalytic scaffolding protein in capsid assembly. J. Supramol. Struct. 1974, 2 (2-4), 202-224.
13. Botstein, D.; Waddell, C. H.; King, J. Mechanism of head assembly and DNA encapsulation in Salmonella phage p22. I. Genes, proteins, structures and DNA maturation. J. Mol. Biol. 1973, 80 (4), 669-695.
14. Galisteo, M. L.; King, J. Conformational transformations in the protein lattice of phage P22 procapsids. Biophys. J. 1993, 65 (1), 227-235.
15. Morais, M. C.; Choi, K. H.; Koti, J. S.; Chipman, P. R.; Anderson, D. L.; Rossmann, M. G. Conservation of the capsid structure in tailed dsDNA bacteriophages: the pseudoatomic structure of phi29. Mol. Cell 2005, 18 (2), 149-159.
16. Fokine, A.; Leiman, P. G.; Shneider, M. M.; Ahvazi, B.; Boeshans, K. M.; Steven, A. C.; Black, L. W.; Mesyanzhinov, V. V.; Rossmann, M. G. Structural and functional similarities between the capsid proteins of bacteriophages T4 and HK97 point to a common ancestry. Proc. Natl Acad. Sci. U.S.A. 2005, 102 (20), 7163-7168.
17. Sinz, A. Chemical cross-linking and mass spectrometry for mapping three-dimensional structures of proteins and protein complexes. J. Mass Spectrom. 2003, 38 (12), 1225-1237.
18. Trester-Zedlitz, M.; Kamada, K.; Burley, S. K.; Fenyo, D.; Chait, B. T.; Muir, T. W. A modular cross-linking approach for exploring protein interactions. J. Am. Chem. Soc. 2003, 125 (9), 2416-2425.
19. Schulz, D. M.; Ihling, C.; Clore, G. M.; Sinz, A. Mapping the topology and determination of a low-resolution three-dimensional structure of the calmodulin-melittin complex by chemical cross-linking and high-resolution FTICRMS: direct demonstration of multiple binding modes. Biochemistry 2004, 43 (16), 4703-4715.
20. Cai, K.; Itoh, Y.; Khorana, H. G. Mapping of contact sites in complex formation between transducin and light-activated rhodopsin by covalent cross-linking: use of a photoactivatable reagent.-[see comment]. Proc. Natl. Acad. Sci. U.S.A. 2001, 98 (9), 4877-4882.
21. Young, M. M.; Tang, N.; Hempel, J. C.; Oshiro, C. M.; Taylor, E. W.; Kuntz, I. D.; Gibson, B. W.; Dollinger, G. High-throughput protein fold identification by using experimental constraints derived from intramolecular cross-links and mass spectrometry. Proc. Natl. Acad. Sci. U.S.A. 2000, 97 (11), 5802-5826.
22. Back, J. W.; de long, L.; Muijsers, A. O.; de Koster, C. G. Chemical cross-linking and mass spectrometry for protein structural modeling. J. Mol. Biol. 2003, 331 (2), 303-313.
23. Green, N. S.; Reisler, E.; Houk, K. N. Quantitative evaluation of the lengths of homobifunctional protein cross-linking reagents used as molecular rulers. Protein Sci. 2001, 10 (7), 1293-1304.
24. Prevelige, P. E., Jr.; Thomas, D.; King, J. Scaffolding protein regulates the polymerization of P22 coat subunits into icosahedral shells in vitro. J. Mol. Biol. 1988, 202 (4), 743-757.
25. Rosenfeld, J.; Capdevielle, J.; Guillemot, J. C.; Ferrara, P. In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal. Biochem. 1992, 203 (1), 173-179.
26. Nepomuceno, A. I.; Muddiman, D. C.; Bergen, H. R., 3rd; Craighead, J. R.; Burke, M. J.; Caskey, P. E.; Allan, J. A. Dual electrospray ionization source for confident generation of accurate mass tags using liquid chromatography Fourier transform ion cyclotron resonance mass spectrometry. Anal. Chem. 2003, 75 (14), 3411-3418.
27. Serwer, P.; Hayes, S. J.; Griess, G. A. Determination of a particle's radius by two-dimensional agarose gel electrophoresis. Anal. Biochem. 1986, 152 (2), 339-345.
28. Thuman-Commike, P. A.; Greene, B.; Malinski, J. A.; Burbea, M.; McGough, A.; Chiu, W.; Prevelige, P. E., Jr. Mechanism of scaffolding-directed virus assembly suggested by comparison of scaffolding-containing and scaffolding-lacking P22 procapsids. Biophys. J. 1999, 76 (6), 3267-3277.
29. Schilling, B.; Row, R. H.; Gibson, B. W.; Guo, X.; Young, M. M. MS2Assign, automated assignment and nomenclature of tandem mass spectra of chemically cross-linked peptides. J. Am. Soc. Mass Spectrom. 2003, 14 (8), 834-850.
30. Lanman, J.; Tuma, R.; Prevelige, P. E., Jr. Identification and characterization of the domain structure of bacteriophage P22 coat protein. Biochemistry 1999, 38 (44), 14614-14623.
31. Tuma, R.; Prevelige, P. E., Jr.; Thomas, G. J., Jr. Mechanism of capsid maturation in a double-stranded DNA virus. Proc. Natl. Acad. Sci. U.S.A. 1998, 95 (17), 9885-9890.
32. Earnshaw, W.; Casjens, S.; Harrison, S. C. Assembly of the head of bacteriophage P22: X-ray diffraction from heads, proheads and related structures. J. Mol. Biol. 1976, 104 (2), 387-410.
33. Conway, J. F.; Wikoff, W. R.; Cheng, N.; Duda, R. L.; Hendrix, R. W.; Johnson, J. E.; Steven, A. C. Virus maturation involving large subunit rotations and local refolding. Science 2001, 292 (5517), 744-748.
34. Zlotnick, A.; Aldrich, R.; Johnson, J. M.; Ceres, P.; Young, M. J. Mechanism of capsid assembly for an icosahedral plant virus. Virology 2000, 277 (2), 450-456.
35. Hendrix, R. W.; Duda, R. L. Bacteriophage HK97 head assembly: a protein ballet. Adv. Virus Res. 1998, 50, 235-288.