Probing Conserved Helical Modules of Portal Complexes by Mass Spectrometry-based Hydrogen/Deuterium Exchange

Journal of Molecular Biology

Volumn 381, Issue 3, 2008, Pages 772-784

  Kang, Sebyung ^a,b   Poliakov, Anton ^a   Sexton, Jennifer ^a   Renfrow, Matthew B ^b,c   Prevelige Jr , Peter E ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

bacteriophage P22; hydrogen exchange; mass spectrometry; portal protein; virus

Indexed keywords

MONOMER;

ARTICLE; COMPARATIVE STUDY; CRYSTAL STRUCTURE; DEUTERIUM HYDROGEN EXCHANGE; IN VITRO STUDY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN INTERACTION;

SIMPLEXVIRUS;

EID: 47949110094     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.03.004     Document Type: Article

References (41)

1. Casjens S., and King J. Virus assembly. Annu. Rev. Biochem. 44 (1975) 555-611
2. Chiu W., Burnett R., and Garcea R. Structural Biology of Viruses (1997), Oxford University Press, New York
3. Sun Y., Parker M.H., Weigele P., Casjens S., Prevelige Jr. P.E., and Krishna N.R. Structure of the coat protein-binding domain of the scaffolding protein from a double-stranded DNA virus. J. Mol. Biol. 297 (2000) 1195-1202
4. Morais M.C., Kanamaru S., Badasso M.O., Koti J.S., Owen B.A., McMurray C.T., et al. Bacteriophage Phi29 scaffolding protein gp7 before and after prohead assembly. Nature Struct. Biol. 10 (2003) 572-576
5. Wikoff W.R., Liljas L., Duda R.L., Tsuruta H., Hendrix R.W., and Johnson J.E. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289 (2000) 2129-2133
6. Fokine A., Leiman P.G., Shneider M.M., Ahvazi B., Boeshans K.M., Steven A.C., et al. Structural and functional similarities between the capsid proteins of bacteriophages T4 and HK97 point to a common ancestry. Proc. Natl Acad. Sci. USA 102 (2005) 7163-7168
7. Jiang W., Li Z., Zhang Z., Baker M.L., Prevelige Jr. P.E., and Chiu W. Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nature Struct. Biol. 10 (2003) 131-135
8. Morais M.C., Choi K.H., Koti J.S., Chipman P.R., Anderson D.L., and Rossmann M.G. Conservation of the capsid structure in tailed dsDNA bacteriophages: the pseudoatomic structure of phi29. Mol. Cell. 18 (2005) 149-159
9. Agirrezabala X., Velazquez-Muriel J.A., Gomez-Puertas P., Scheres S.H.W., Carazo J.M., and Carrascosa J.L. Quasi-atomic model of bacteriophage T7 procapsid shell: insights into the structure and evolution of a basic fold. Structure 15 (2007) 461-472
10. Baker M.L., Jiang W., Rixon F.J., and Chiu W. Common ancestry of herpesviruses and tailed DNA bacteriophages. J. Virol. 79 (2005) 14967-14970
11. Jiang W., Chang J., Jakana J., Weigele P., King J., and Chiu W. Structure of epsilon15 bacteriophage reveals genome organization and DNA packaging/injection apparatus. Nature 439 (2006) 612-616
12. Lurz R., Orlova E.V., Gunther D., Dube P., Droge A., Weise F., et al. Structural organisation of the head-to-tail interface of a bacterial virus. J. Mol. Biol. 310 (2001) 1027-1037
13. Carrascosa J.L., Carazo J.M., Ibanez C., and Santisteban A. Structure of phage phi 29 connector protein assembled in vivo. Virology 141 (1985) 190-200
14. Donate L.E., Herranz L., Secilla J.P., Carazo J.M., Fujisawa H., and Carrascosa J.L. Bacteriophage T3 connector: three-dimensional structure and comparison with other viral head-tail connecting regions. J. Mol. Biol. 201 (1988) 91-100
15. Kochan J., Carrascosa J.L., and Murialdo H. Bacteriophage lambda preconnectors: purification and structure. J. Mol. Biol. 174 (1984) 433-447
16. Tang L., Marion W.R., Cingolani G., Prevelige P.E., and Johnson J.E. Three-dimensional structure of the bacteriophage P22 tail machine. EMBO J. 24 (2005) 2087-2095
17. Lander G.C., Tang L., Casjens S.R., Gilcrease E.B., Prevelige P., Poliakov A., et al. The structure of an infectious P22 virion shows the signal for headful DNA packaging. Science 312 (2006) 1791-1795
18. Agirrezabala A., Martin-Benito J., Caston J.R., Miranda R., Valpuesta J.M., and Carrascosa J.L. Maturation of phage T7 involves structural modification of both shell and inner core components. The EMBO J. 24 (2005) 3820-3829
19. Simpson A.A., Tao Y., Leiman P.G., Badasso M.O., He Y., Jardine P.J., et al. Structure of the bacteriophage Phi29 DNA packaging motor. Nature 408 (2000) 745-750
20. Lebedev A.A., Krause M.H., Isidro A.L., Vagin A.A., Orlova E.V., Turner J., et al. Structural framework for DNA translocation via the viral portal protein. EMBO J. 26 (2007) 1984-1994
21. Orlova E.V., Gowen B., Droge A., Stiege A., Weise F., Lurz R., et al. Structure of a viral DNA gatekeeper at 10 Å resolution by cryo-electron microscopy. EMBO J. 22 (2003) 1255-1262
22. Cardone G., Winkler D.C., Trus B.L., Cheng N., Heuser J.E., Newcomb W.W., et al. Visualization of the herpes simplex virus portal in situ by cryo-electron tomography. Virology 361 (2007) 426-434
23. Chang J.T., Schmid M.F., Rixon F.J., and Chiu W. Electron cryotomography reveals the portal in the herpesvirus capsid. J. Virol. 81 (2007) 2065-2068
24. Rodriguez-Casado A., Moore S.D., P.E., P., and Thomas G.J. Structure of bacteriophage P22 portal protein in relation to assembly: investigation by Raman spectroscopy. Biochemstry 40 (2001) 13583-13591
25. Englander S.W., and Kallenbach N.R. Hydrogen exchange and structural dynamics of proteins and nucleic acids. Quart. Rev. Biophys. 16 (1983) 521-655
26. Truhlar S.M.E., Croy C.H., Torpey J.W., Koeppe J.R., and Komives E.A. Solvent accessibility of protein surfaces by amide H/2H exchange MALDI-TOF mass spectrometry. J. Am. Soc. Mass. Spectrom. 17 (2006) 1490-1497
27. Zhang Z., and Smith D.L. Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation. Protein Sci. 2 (1993) 522-531
28. Truhlar S.M.E., Torpey J.W., and Komives E.A. Regions of IκBα that are critical for its inhibition of NF-κB·DNA interaction fold upon binding to NF-κB. Proc. Natl Acad. Sci. USA 103 (2006) 18951-18956
29. Moore S.D., and Prevelige Jr. P.E. Structural transformations accompanying the assembly of bacteriophage P22 portal protein rings in vitro. J. Biol. Chem. 276 (2001) 6779-6788
30. Poliakov A., Duijn E.v., Lander G., Fu C.-y., Johnson J.E., Prevelige J., et al. Macromolecular mass spectrometry and electron microscopy as complementary tools for investigation of the heterogeneity of bacteriophage portal assemblies. J. Struct. Biol. 157 (2007) 371-383
31. Agirrezabala X., Martin-Benito J., Valle M., Gonzalez J.M., Valencia A., Valpuesta J.M., and Carrascosa J.L. Structure of the connector of bacteriophage T7 at 8 Å resolution: structural homologies of a basic component of a DNA translocating machinery. J. Mol. Biol. 347 (2005) 895-902
32. Jekow P., Behlke J., Tichelaar W., Lurz R., Regalla M., Hinrichs W., and Tavares P. Effect of the ionic environment on the molecular structure of bacteriophage SPP1 portal protein. Eur. J. Biochem. 264 (1999) 724-735
33. Orlova E.V., Dube P., Beckmann E., Zemlin F., Lurz R., Trautner T.A., et al. Structure of the 13-fold symmetric portal protein of bacteriophage SPP1. Nature Struct. Biol. 6 (1999) 842-846
34. Valpuesta J.M., Sousa N., Barthelemy I., Fernandez J.J., Fujisawa H., Ibarra B., and Carrascosa J.L. Structural analysis of the bacteriophage T3 head-to-tail connector. J. Struct. Biol. 131 (2000) 146-155
35. Trus B.L., Cheng N., Newcomb W.W., Homa F.L., Brown J.C., and Steven A.C. Structure and polymorphism of the UL6 portal protein of herpes simplex virus type 1. J. Virol. 78 (2004) 12668-12671
36. Lanman J., Lam T.T., Barnes S., Sakalian M., Emmett M.R., Marshall A.G., and Prevelige Jr. P.E. Identification of novel interactions in HIV-1 capsid protein assembly by high-resolution mass spectrometry. J. Mo. Biol. 325 (2003) 759-772
37. Kang S., and Prevelige Jr. P.E. Domain study of bacteriophage p22 coat protein and characterization of the capsid lattice transformation by hydrogen/deuterium exchange. J. Mol. Biol. 347 (2005) 935-948
38. Lisal J., Lam T.T., Kainov D.E., Emmett M.R., Marshall A.G., and Tuma R. Functional visualization of viral molecular motor by hydrogen-deuterium exchange reveals transient states. Nature Struct. Mol. Biol. 12 (2005) 460-466
39. Wang L., Lane L.C., and Smith D.L. Detecting structural changes in viral capsids by hydrogen exchange and mass spectrometry. Protein Sci. 10 (2001) 1234-1243
40. Fu C., and Prevelige P. Dynamic motions of free and bound phi29 scaffolding protein identified by hydrogen deuterium exchange mass spectrometry. Protein Sci. 15 (2006) 731-743
41. Ibanez C., Garcia J.A., Carrascosa J.L., and Salas M. Overproduction and purification of the connector protein of Bacillus subtilis phage Phi29. Nucleic Acids Res. 12 (1984) 2351-2365