Bacteriophage HK97 capsid assembly is a premier model system for studying
aspects of protein assembly mechanisms. Maturation of the head protein
of HK97 includes interesting interactions with chaperonins, assembly into
interconvertible hexamers and pentamers, assembly into Prohead I together
with portal and protease proteins, cleavage of the head protein and protease
within the interior of the structure to create a new intermediate, Prohead
II, expansion and interlinking of protein subunit chains, and the formation
of novel covalent inter-peptide crosslinks.
The HK97 Head Assembly Pathway
The HK97 head is assembled from minor proteins gp3 (47 kDa), gp4 (25kDa),
and the major head protein, gp5 (42kDa). The initial steps require the
host chaperones GroEL & GroES and ATP. Prohead I is the first large
intermediate and is converted to Prohead II when gp5 is cleaved from 42kDa
to 31kDa under the control of gp4. The portion of gp5 that is lost is called
the delta region and lies inside the shell. Prohead II will mature and expand into
a mature Head, usually at the time of DNA packaging. During expansion,
reactive sites are created that cross-link gp5 subunits to adjacent
subunits until all of the subunits are crosslinked in Head II.
The above surface rendered images are colorized
versions of images made by James Conway from micrographs taken by Naiqian
Cheng - see collaborations
and J.Mol. Biol. 253: 86-99.
Electron micrograph of Bacteriophage HK97 negatively stained with uranyl acetate
return to or enter Bob Duda's web site
Publications about Bacteriophage HK97
- Solution NMR studies of the maturation intermediates of a 13 MDa viral capsid.
- Szymczyna, B. R., L. Gan, J. E. Johnson, and J. R. Williamson.
- 2007. J Am Chem Soc 129:7867-76.
- A thermally induced phase transition in a viral capsid transforms the hexamers, leaving the pentamers unchanged.
- Conway, J. F., N. Cheng, P. D. Ross, R. W. Hendrix, R. L. Duda, and A. C. Steven.
- 2007. J Struct Biol 158:224-32.
- Time-resolved molecular dynamics of bacteriophage HK97 capsid maturation interpreted by electron cryo-microscopy and X-ray crystallography.
- Wikoff, W. R., J. F. Conway, J. Tang, K. K. Lee, L. Gan, N. Cheng, R. L. Duda, R. W. Hendrix, A. C. Steven, and J. E. Johnson.
- 2006. J Struct Biol 153:300-6.
- Capsid conformational sampling in HK97 maturation visualized by X-ray crystallography and cryo-EM.
- Gan, L., J. A. Speir, J. F. Conway, G. Lander, N. Cheng, B. A. Firek, R. W. Hendrix, R. L. Duda, L. Liljas, and J. E. Johnson.
- 2006. Structure 14:1655-65.
- Crosslinking in viral capsids via tiling theory.
- Twarock, R., and R. W. Hendrix.
- 2005. J Theor Biol.
- Diversity and identity of mechanical properties of icosahedral viral capsids studied with elastic network normal mode analysis.
- Tama, F., and C. L. Brooks, 3rd.
- 2005. J Mol Biol 345:299-314.
- Crosslinking renders bacteriophage HK97 capsid maturation irreversible and effects an essential stabilization.
- Ross, P. D., N. Cheng, J. F. Conway, B. A. Firek, R. W. Hendrix, R. L. Duda, and A. C. Steven.
- 2005. Embo J 24:1352-63.
- Maturation dynamics of bacteriophage HK97 capsid.
- Rader, A. J., D. H. Vlad, and I. Bahar.
- 2005. Structure (Camb) 13:413-21.
- Control of virus assembly: HK97 "Whiffleball" mutant capsids without pentons.
- Li, Y., J. F. Conway, N. Cheng, A. C. Steven, R. W. Hendrix, and R. L. Duda.
- 2005. J Mol Biol 348:167-82.
- Cooperative reorganization of a 420 subunit virus capsid.
- Lee, K. K., H. Tsuruta, R. W. Hendrix, R. L. Duda, and J. E. Johnson.
- 2005. J Mol Biol 352:723-35.
- Rigid-cluster models of conformational transitions in macromolecular machines and assemblies.
- Kim, M. K., R. L. Jernigan, and G. S. Chirikjian.
- 2005. Biophys J 89:43-55.
- Bacteriophage HK97: assembly of the capsid and evolutionary connections.
- Hendrix, R. W.
- 2005. Adv Virus Res 64:1-14.
- Elastic network models for understanding biomolecular machinery: from enzymes to supramolecular assemblies.
- Chennubhotla, C., A. J. Rader, L. W. Yang, and I. Bahar.
- 2005. Phys Biol 2:S173-80.
- Evidence that a local refolding event triggers maturation of HK97 bacteriophage capsid.
- Lee, K. K., L. Gan, H. Tsuruta, R. W. Hendrix, R. L. Duda, and J. E. Johnson.
- 2004. J Mol Biol 340:419-33.
- Control of crosslinking by quaternary structure changes during bacteriophage HK97 maturation.
- Gan, L., J. F. Conway, B. A. Firek, N. Cheng, R. W. Hendrix, A. C. Steven, J. E. Johnson, and R. L. Duda.
- 2004. Mol Cell 14:559-69.
- Domain structures and roles in bacteriophage HK97 capsid assembly and maturation.
- Benevides, J. M., P. Bondre, R. L. Duda, R. W. Hendrix, and G. J. Thomas, Jr.
- 2004. Biochemistry 43:5428-36.
- Crystallization and preliminary analysis of a dsDNA bacteriophage capsid intermediate: Prohead II of HK97.
- Wikoff, W. R., Z. Che, R. L. Duda, R. W. Hendrix, and J. E. Johnson.
- 2003. Acta Crystallogr D Biol Crystallogr 59:2060-4.
- An elastic network model of HK97 capsid maturation.
- Kim, M. K., R. L. Jernigan, and G. S. Chirikjian.
- 2003. J Struct Biol 143:107-17.
- The refined structure of a protein catenane: the HK97 bacteriophage capsid at 3.44 A resolution.
- Helgstrand, C., W. R. Wikoff, R. L. Duda, R. W. Hendrix, J. E. Johnson, and L. Liljas.
- 2003. J Mol Biol 334:885-99.
- Virus maturation involving large subunit rotations and local refolding.
- Conway, J. F., W. R. Wikoff, N. Cheng, R. L. Duda, R. W. Hendrix, J. E. Johnson, and A. C. Steven.
- 2001. Science 292:744-8.
- High-temperature protein mass mapping using a thermophilic protease.
- Bark, S. J., N. Muster, J. R. Yates, 3rd, and G. Siuzdak.
- 2001. J Am Chem Soc 123:1774-5.
- Topologically linked protein rings in the bacteriophage HK97 capsid.
- Wikoff, W. R., L. Liljas, R. L. Duda, H. Tsuruta, R. W. Hendrix, and J. E. Johnson.
- 2000. Science 289:2129-33.
- Maturation dynamics of a viral capsid: visualization of transitional intermediate states.
- Lata, R., J. F. Conway, N. Cheng, R. L. Duda, R. W. Hendrix, W. R. Wikoff, J. E. Johnson, H. Tsuruta, and A. C. Steven.
- 2000. Cell 100:253-63.
- Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages.
- Juhala, R. J., M. E. Ford, R. L. Duda, A. Youlton, G. F. Hatfull, and R. W. Hendrix.
- 2000. J Mol Biol 299:27-51.
- Virus assembly: Imaging a molecular machine.
- Wikoff, W. R., and J. E. Johnson.
- 1999. Curr Biol 9:R296-300.
- Crystallographic analysis of the dsDNA bacteriophage HK97 mature empty capsid.
- Wikoff, W. R., R. L. Duda, R. W. Hendrix, and J. E. Johnson.
- 1999. Acta Crystallogr D Biol Crystallogr 55 (Pt 4):763-71.
- Family values in the age of genomics: comparative analyses of temperate bacteriophage HK022.
- Weisberg, R. A., M. E. Gottesmann, R. W. Hendrix, and J. W. Little.
- 1999. Annu Rev Genet 33:565-602.
- Crystallization and preliminary X-ray analysis of the dsDNA bacteriophage HK97 mature empty capsid.
- Wikoff, W. R., R. L. Duda, R. W. Hendrix, and J. E. Johnson.
- 1998. Virology 243:113-8.
- Macromolecular assembly: chainmail stabilization of a viral capsid.
- Johnson, J. E., and W. R. Wikoff.
- 1998. Curr Biol 8:R914-7.
- Bacteriophage HK97 head assembly: a protein ballet.
- Hendrix, R. W., and R. L. Duda.
- 1998. Adv Virus Res 50:235-88.
- Protein chainmail: catenated protein in viral capsids.
- Duda, R. L.
- 1998. Cell 94:55-60.
- Assembly in vitro of bacteriophage HK97 proheads.
- Xie, Z., and R. W. Hendrix.
- 1995. J Mol Biol 253:74-85.
- Bacteriophage HK97 head assembly.
- Duda, R. L., K. Martincic, Z. Xie, and R. W. Hendrix.
- 1995. FEMS Microbiol Rev 17:41-6.
- Genetic basis of bacteriophage HK97 prohead assembly.
- Duda, R. L., K. Martincic, and R. W. Hendrix.
- 1995. J Mol Biol 247:636-47.
- Structural transitions during bacteriophage HK97 head assembly.
- Duda, R. L., J. Hempel, H. Michel, J. Shabanowitz, D. Hunt, and R. W. Hendrix.
- 1995. J Mol Biol 247:618-35.
- Complexes between chaperonin GroEL and the capsid protein of bacteriophage HK97.
- Ding, Y., R. L. Duda, R. W. Hendrix, and J. M. Rosenberg.
- 1995. Biochemistry 34:14918-31.
- Proteolytic and conformational control of virus capsid maturation: the bacteriophage HK97 system.
- Conway, J. F., R. L. Duda, N. Cheng, R. W. Hendrix, and A. C. Steven.
- 1995. J Mol Biol 253:86-99.
- Bacteriophage HK97 structure: wholesale covalent cross-linking between the major head shell subunits.
- Popa, M. P., T. A. McKelvey, J. Hempel, and R. W. Hendrix.
- 1991. J Virol 65:3227-37.
- Host range, immunity and antigenic properties of lambdoid coliphage HK97.
- Dhillon, E. K., T. S. Dhillon, A. N. Lai, and S. Linn.
- 1980. J Gen Virol 50:217-20.