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Protein chainmail variants in dsDNA viruses

1 Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, California 90095, USA;
2 California NanoSystems Institute (CNSI), University of California, Los Angeles (UCLA), Los Angeles, CA, 90095, USA

Special Issues: Structural analysis of macromolecules using Cryo electron microscopy

First discovered in bacteriophage HK97, biological chainmail is a highly stable system formed by concatenated protein rings. Each subunit of the ring contains the HK97-like fold, which is characterized by its submarine-like shape with a 5-stranded β sheet in the axial (A) domain, spine helix in the peripheral (P) domain, and an extended (E) loop. HK97 capsid consists of covalently-linked copies of just one HK97-like fold protein and represents the most effective strategy to form highly stable chainmail needed for dsDNA genome encapsidation. Recently, near-atomic resolution structures enabled by cryo electron microscopy (cryoEM) have revealed a range of other, more complex variants of this strategy for constructing dsDNA viruses. The first strategy, exemplified by P22-like phages, is the attachment of an insertional (I) domain to the core 5-stranded β sheet of the HK97-like fold. The atomic models of the Bordetella phage BPP-1 showcases an alternative topology of the classic HK97 topology of the HK97-like fold, as well as the second strategy for constructing stable capsids, where an auxiliary jellyroll protein dimer serves to cement the non-covalent chainmail formed by capsid protein subunits. The third strategy, found in lambda-like phages, uses auxiliary protein trimers to stabilize the underlying non-covalent chainmail near the 3-fold axis. Herpesviruses represent highly complex viruses that use a combination of these strategies, resulting in four-level hierarchical organization including a non-covalent chainmail formed by the HK97-like fold domain found in the floor region. A thorough understanding of these structures should help unlock the enigma of the emergence and evolution of dsDNA viruses and inform bioengineering efforts based on these viruses.
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References

1. Duda RL (1998) Protein Chainmail: Catenated Protein in Viral Capsids. Cell 94: 55-60.

2. Wikoff WR, Liljas L, Duda RL, et al. (2000) Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289: 2129-2133.    

3. Akita F, Chong KT, Tanaka H, Y et al. (2007) The Crystal Structure of a Virus-like Particle from the Hyperthermophilic Archaeon Pyrococcus furiosus Provides Insight into the Evolution of Viruses. J Mol Biol 368: 1469-1483.    

4. Sutter M, Boehringer D, Gutmann S, et al. (2008) Structural basis of enzyme encapsulation into a bacterial nanocompartment. Nat Struct Mol Biol 15: 939-947.    

5. Gelbart WM, Knobler CM (2009) Virology. Pressurized viruses. Science 323: 1682-1683.

6. Zhang X, Guo H, Jin L, et al. (2013) A new topology of the HK97-like fold revealed in Bordetella bacteriophage by cryoEM at 3.5 A resolution. eLife 2: e01299.

7. Zhou ZH, Hui WH, Shah S, et al. (2014) Four Levels of Hierarchical Organization, Including Noncovalent Chainmail, Brace the Mature Tumor Herpesvirus Capsid against Pressurization. Struct Lond Engl 1993.

8. Lander GC, Evilevitch A, Jeembaeva M, et al. (2008) Bacteriophage lambda stabilization by auxiliary protein gpD: timing, location, and mechanism of attachment determined by cryoEM. Struct Lond Engl 1993 16: 1399-1406.

9. Parent KN, Khayat R, Tu LH, et al. (2010) P22 coat protein structures reveal a novel mechanism for capsid maturation: stability without auxiliary proteins or chemical crosslinks. Struct Lond Engl 1993 18: 390-401.

10. Baker ML, Jiang W, Rixon FJ, et al. (2005) Common ancestry of herpesviruses and tailed DNA bacteriophages. J Virol 79: 14967-14970.    

11. Tso D, Hendrix RW, Duda RL (2014) Transient contacts on the exterior of the HK97 procapsid that are essential for capsid assembly. J Mol Biol 426: 2112-2129.    

12. Prevelige Jr PE (2008) Send for Reinforcements! Conserved Binding of Capsid Decoration Proteins. Structure 16: 1292-1293.    

13. Rizzo AA, Suhanovsky MM, Baker ML, et al. (2014). Multiple functional roles of the accessory I-domain of bacteriophage P22 coat protein revealed by NMR structure and CryoEM modeling. Struct. Lond Engl 1993 22: 830-841.

14. Chen D-H, Baker ML, Hryc CF, et al. (2011) Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus. Proc Natl Acad Sci 108: 1355-1360.    

15. Parent KN, Gilcrease EB, Casjens SR, et al. (2012) Structural evolution of the P22-like phages: Comparison of Sf6 and P22 procapsid and virion architectures. Virology 427: 177-188.    

16. Parent KN, Tang J, Cardone G, et al. (2014). Three-dimensional reconstructions of the bacteriophage CUS-3 virion reveal a conserved coat protein I-domain but a distinct tailspike receptor-binding domain. Virology 464-465: 55-66.

17. Guo F, Liu Z, Fang P-A, et al. (2014) Capsid expansion mechanism of bacteriophage T7 revealed by multistate atomic models derived from cryo-EM reconstructions. Proc Natl Acad Sci 111: E4606-E4614.    

18. Fokine A, Leiman PG, Shneider MM, et al. (2005) 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 102: 7163-7168.    

19. Yang F, Forrer P, Dauter Z, et al. (2000) Novel fold and capsid-binding properties of the λ-phage display platform protein gpD. Nat Struct Mol Biol 7: 230-237.    

20. Baker ML, Hryc CF, Zhang Q, et al. (2013) Validated near-atomic resolution structure of bacteriophage epsilon15 derived from cryo-EM and modeling. Proc Natl Acad Sci U S A 110: 12301-12306.    

21. Iwai H, Forrer P, Plückthun A, et al. (2005) NMR solution structure of the monomeric form of the bacteriophage λ capsid stabilizing protein gpD. J Biomol NMR 31: 351-356.    

22. Morais MC, Choi KH, Koti JS, et al. (2005) Conservation of the Capsid Structure in Tailed dsDNA Bacteriophages: the Pseudoatomic Structure of ϕ29. Mol Cell 18: 149-159.    

23. Roizman B, Knipe DM, Whitley RJ (2007) Herpes simplex viruses. In Fields Virology, (Philadelphia: Lippincott-Williams & Wilkins), 2502-1601.

24. Mocarski ES, Shenk T, Pass RF (2007) Cytomegaloviruses. In Fields Virology, (Philadelphia: Lippincott-Williams & Wilkins), 2702-2772.

25. Chang Y, Cesarman E, Pessin MS, et al. (1994). Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266: 1865-1869.    

26. Ganem D (2007) Kaposi's sarcoma-associated herpesvirus. In Fields Virology, (Philadelphia: Lippincott-Williams & Wilkins), 2847-2888.

27. Rickinson AB, Kieff E (2007) Epstein-Barr Virus. In Fields Virology, (Philadelphia: Lippincott-Williams & Wilkins), 2656-2700.

28. Dai X, Gong D, Wu T-T, et al. (2014) Organization of capsid-associated tegument components in Kaposi's sarcoma-associated herpesvirus. J Virol 88: 12694-12702.    

29. Hui WH, Tang Q, Liu H, et al. (2013) Protein interactions in the murine cytomegalovirus capsid revealed by cryoEM. Protein Cell 4: 833-845.    

30. Forterre P, Krupovic M (2012) The Origin of Virions and Virocells: The Escape Hypothesis Revisited. In Viruses: Essential Agents of Life, G. Witzany, ed. (Springer Netherlands), 43-60.

31. Heinemann J, Maaty WS, Gauss GH, et al. (2011) Fossil record of an archaeal HK97-like provirus. Virology 417: 362-368.    

32. Bujnicki JM (2002) Sequence permutations in the molecular evolution of DNA methyltransferases. BMC Evol Biol 2: 3.    

33. Peisajovich SG, Rockah L, Tawfik DS (2006) Evolution of new protein topologies through multistep gene rearrangements. Nat Genet 38: 168-174.    

34. Vogel C, Morea V (2006) Duplication, divergence and formation of novel protein topologies. Bio Essays 28: 973-978.

Copyright Info: © 2015, Z. Hong Zhou, et al., licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution Licese (http://creativecommons.org/licenses/by/4.0)

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