Bacteriophage HK97 Capsid Assembly and Maturation (original) (raw)
Abstract
The Escherichia coli phage HK97 has provided a productive experimental system for investigating how virus capsids are assembled from their protein components and how the assembled capsids mature to their final form. Aspects of the process for which the HK97 system has been particularly informative include assembly of the icosahedral capsid shell from the component proteins, structure of the capsid subunits and of the entire capsid as it progresses through its maturation, and the mechanism of the covalent cross-linking that links the subunits together into viral chain mail. The structural dynamics of the maturation as well as the energetics that drives maturation forward are beginning to be understood.
Similar content being viewed by others
References
- Baker ML, Jiang W, Rixon FJ, Chiu W (2005) Common ancestry of herpesviruses and tailed DNA bacteriophages. J Virol 79:14967–14970
Article PubMed CAS Google Scholar - Bamford DH, Grimes JM, Stuart DI (2005) What does structure tell us about virus evolution? Curr Opin Struct Biol 15:655–663
Article PubMed CAS Google Scholar - Benevides JM, Bondre P, Duda RL, Hendrix RW, Thomas GJ Jr (2004) Domain structures and roles in bacteriophage HK97 capsid assembly and maturation. Biochemistry 43:5428–5436
Article PubMed CAS Google Scholar - Caspar DL, Klug A (1962) Physical principles in the construction of regular viruses. Cold Spring Harb Symp Quant Biol 27:1–24
Article PubMed CAS Google Scholar - Conway JF, Duda RL, Cheng N, Hendrix RW, Steven AC (1995) Proteolytic and conformational control of virus capsid maturation: the bacteriophage HK97 system. J Mol Biol 253:86–99
Article PubMed CAS Google Scholar - Conway JF, Wikoff WR, Cheng N, Duda RL, Hendrix RW, Johnson JE, Steven AC (2001) Virus maturation involving large subunit rotations and local refolding. Science 292:744–748
Article PubMed CAS Google Scholar - Conway JF, Cheng N, Ross PD, Hendrix RW, Duda RL, Steven AC (2007) A thermally induced phase transition in a viral capsid transforms the hexamers, leaving the pentamers unchanged. J Struct Biol 158:224–232
Article PubMed CAS Google Scholar - Dhillon EK, Dhillon TS, Lai AN, Linn S (1980) Host range, immunity and antigenic properties of lambdoid coliphage HK97. J Gen Virol 50:217–220
Article PubMed CAS Google Scholar - Dierkes LE, Peebles CL, Firek BA, Hendrix RW, Duda RL (2009) Mutational analysis of a conserved glutamic acid required for self-catalyzed cross-linking of bacteriophage HK97 capsids. J Virol 83:2088–2098
Article PubMed CAS Google Scholar - Ding Y, Duda RL, Hendrix RW, Rosenberg JM (1995) Complexes between chaperonin GroEL and the capsid protein of bacteriophage HK97. Biochemistry 34:14918–14931
Article PubMed CAS Google Scholar - Duda R (1998) Protein chainmail: catenated protein in viral capsids. Cell 94:55–60
Google Scholar - Duda RL, Hempel J, Michel H, Shabanowitz J, Hunt D, Hendrix RW (1995a) Structural transitions during bacteriophage HK97 head assembly. J Mol Biol 247:618–635
PubMed CAS Google Scholar - Duda RL, Martincic K, Hendrix RW (1995b) Genetic basis of bacteriophage HK97 prohead assembly. J Mol Biol 247:636–647
PubMed CAS Google Scholar - Duda RL, Martincic K, Xie Z, Hendrix RW (1995c) Bacteriophage HK97 head assembly. FEMS Microbiol Rev 17:41–46
Article PubMed CAS Google Scholar - Duda RL, Hendrix RW, Huang WM, Conway JF (2006) Shared architecture of bacteriophage SPO1 and herpesvirus capsids. Curr Biol 16:R11–R13
Article PubMed CAS Google Scholar - Galisteo ML, King J (1993) Conformational transformations in the protein lattice of phage P22 procapsids. Biophys J 65:227–235
Article PubMed CAS Google Scholar - Gan L, Conway JF, Firek BA, Cheng N, Hendrix RW, Steven AC, Johnson JE, Duda RL (2004) Control of crosslinking by quaternary structure changes during bacteriophage HK97 maturation. Mol Cell 14:559–569
Article PubMed CAS Google Scholar - Gan L, Speir JA, Conway JF, Lander G, Cheng N, Firek BA, Hendrix RW, Duda RL, Liljas L, Johnson JE (2006) Capsid conformational sampling in HK97 maturation visualized by X-ray crystallography and cryo-EM. Structure 14:1655–1665
Article PubMed Google Scholar - Gertsman I, Gan L, Guttman M, Lee K, Speir JA, Duda RL, Hendrix RW, Komives EA, Johnson JE (2009) An unexpected twist in viral capsid maturation. Nature 458:646–650
Article PubMed CAS Google Scholar - Gertsman I, Fu CY, Huang R, Komives EA, Johnson JE (2010) Critical salt bridges guide capsid assembly, stability, and maturation behavior in bacteriophage HK97. Mol Cell Proteomics 9:1752–1763
Article PubMed CAS Google Scholar - Helgstrand C, Wikoff WR, Duda RL, Hendrix RW, Johnson JE, Liljas L (2003) The refined structure of a protein catenane: the HK97 bacteriophage capsid at 3.44 A resolution. J Mol Biol 334:885–899
Article PubMed CAS Google Scholar - Hendrix RW (1999) Evolution: the long evolutionary reach of viruses. Curr Biol 9:R914–R917
Article PubMed CAS Google Scholar - Hendrix RW (2002) Bacteriophages: evolution of the majority. Theor Popul Biol 61:471–480
Article PubMed Google Scholar - Huang RK, Khayat R, Lee KK, Gertsman I, Duda RL, Hendrix RW, Johnson JE (2011) The prohead-I structure of bacteriophage HK97: implications for scaffold-mediated control of particle assembly and maturation. J Mol Biol 408:541–554
Article PubMed CAS Google Scholar - Johnson JE (2010) Virus particle maturation: insights into elegantly programmed nanomachines. Curr Opin Struct Biol 20:210–216
Article PubMed CAS Google Scholar - Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, Hendrix RW (2000) Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299:27–51
Article PubMed CAS Google Scholar - Kang HJ, Coulibaly F, Clow F, Proft T, Baker EN (2007) Stabilizing isopeptide bonds revealed in gram-positive bacterial pilus structure. Science 318:1625–1628
Article PubMed CAS Google Scholar - Katsura I, Hendrix RW (1984) Length determination in bacteriophage lambda tails. Cell 39:691–698
Article PubMed CAS Google Scholar - Lata R, Conway JF, Cheng N, Duda RL, Hendrix RW, Wikoff WR, Johnson JE, Tsuruta H, Steven AC (2000) Maturation dynamics of a viral capsid: visualization of transitional intermediate states. Cell 100:253–263
Article PubMed CAS Google Scholar - Lee KK, Tsuruta H, Hendrix RW, Duda RL, Johnson JE (2005) Cooperative reorganization of a 420 subunit virus capsid. J Mol Biol 352:723–735
Article PubMed CAS Google Scholar - Lee KK, Gan L, Tsuruta H, Moyer C, Conway JF, Duda RL, Hendrix RW, Steven AC, Johnson JE (2008) Virus capsid expansion driven by the capture of mobile surface loops. Structure 16:1491–1502
Article PubMed CAS Google Scholar - Li Y, Conway JF, Cheng N, Steven AC, Hendrix RW, Duda RL (2005) Control of virus assembly: HK97 “Whiffleball” mutant capsids without pentons. J Mol Biol 348:167–182
Article PubMed CAS Google Scholar - Nemecek D, Overman SA, Hendrix RW, Thomas GJ Jr (2009) Unfolding thermodynamics of the delta-domain in the prohead I subunit of phage HK97: determination by factor analysis of Raman spectra. J Mol Biol 385:628–641
Article PubMed CAS Google Scholar - Popa MP, McKelvey TA, Hempel J, Hendrix RW (1991) Bacteriophage HK97 structure: wholesale covalent cross-linking between the major head shell subunits. J Virol 65:3227–3237
PubMed CAS Google Scholar - Ross PD, Cheng N, Conway JF, Firek BA, Hendrix RW, Duda RL, Steven AC (2005) Crosslinking renders bacteriophage HK97 capsid maturation irreversible and effects an essential stabilization. EMBO J 24:1352–1363
Article PubMed CAS Google Scholar - Sternberg N, Weisberg R (1977) Packaging of coliphage lambda DNA II. The role of the D protein. J Mol Biol 117:733–759
Google Scholar - Suttle CA (2007) Marine viruses – major players in the global ecosystem. Nat Rev Microbiol 5:801–812
Article PubMed CAS Google Scholar - Tong L (2002) Viral proteases. Chem Rev 102:4609–4626
Article PubMed CAS Google Scholar - Wikoff WR, Liljas L, Duda RL, Tsuruta H, Hendrix RW, Johnson JE (2000) Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289:2129–2133
Article PubMed CAS Google Scholar - Wikoff WR, Che Z, Duda RL, Hendrix RW, Johnson JE (2003) Crystallization and preliminary analysis of a dsDNA bacteriophage capsid intermediate: prohead II of HK97. Acta Crystallogr D Biol Crystallogr 59:2060–2064
Article PubMed Google Scholar - Xie Z, Hendrix RW (1995) Assembly in vitro of bacteriophage HK97 proheads. J Mol Biol 253:74–85
Article PubMed CAS Google Scholar
Acknowledgments
The work described here is the product of a multilaboratory collaboration involving not only the two authors of this chapter but also Alasdair Steven, Bob Duda, and James Conway, as well as numerous graduate and undergraduate students, postdocs, and technical staff from all of our labs. There have been many important contributions as well from colleagues not as directly associated with the central “HK97 Cabal,” including Lars Liljas, Philip Ross, George Thomas, Hiro Tsuruta, and their associates. Credit for our current understanding of HK97 capsid assembly and maturation is jointly owned. Work on this topic in the labs of the two authors of this chapter has been supported by NIH grants R01-GM47795 (RWH) and R01-AI40101 and R01-GM54076 (JEJ).
Author information
Authors and Affiliations
- Department of Biological Sciences, Pittsburgh Bacteriophage Institute, University of Pittsburgh, Pittsburgh, PA, 15260, USA
Roger W. Hendrix - Department of Molecular Biology, MB31, The Scripps Research Institute, 10550 N. Torrey Pines Road, La Jolla, CA, 92037, USA
John E. Johnson
Authors
- Roger W. Hendrix
You can also search for this author inPubMed Google Scholar - John E. Johnson
You can also search for this author inPubMed Google Scholar
Corresponding author
Correspondence toRoger W. Hendrix .
Editor information
Editors and Affiliations
- Dept. Biological Sciences, Purdue University, W. State St. 915, West Lafayette, 47907-2054, Indiana, USA
Michael G. Rossmann - Dept. Biology, Catholic University of America, Washington, 20064, District of Columbia, USA
Venigalla B. Rao
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media, LLC
About this chapter
Cite this chapter
Hendrix, R.W., Johnson, J.E. (2012). Bacteriophage HK97 Capsid Assembly and Maturation. In: Rossmann, M., Rao, V. (eds) Viral Molecular Machines. Advances in Experimental Medicine and Biology, vol 726. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-0980-9\_15
Download citation
- .RIS
- .ENW
- .BIB
- DOI: https://doi.org/10.1007/978-1-4614-0980-9\_15
- Published: 08 November 2011
- Publisher Name: Springer, Boston, MA
- Print ISBN: 978-1-4614-0979-3
- Online ISBN: 978-1-4614-0980-9
- eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)