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Protein chainmail variants in dsDNA viruses

  • Received: 24 February 2015 Accepted: 14 June 2015 Published: 17 June 2015
  • 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.

    Citation: Z. Hong Zhou, Joshua Chiou. Protein chainmail variants in dsDNA viruses[J]. AIMS Biophysics, 2015, 2(2): 200-218. doi: 10.3934/biophy.2015.2.200

    Related Papers:

  • 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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    [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. doi: 10.1126/science.289.5487.2129
    [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. doi: 10.1016/j.jmb.2007.02.075
    [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. doi: 10.1038/nsmb.1473
    [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. doi: 10.1128/JVI.79.23.14967-14970.2005
    [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. doi: 10.1016/j.jmb.2014.03.009
    [12] Prevelige Jr PE (2008) Send for Reinforcements! Conserved Binding of Capsid Decoration Proteins. Structure 16: 1292-1293. doi: 10.1016/j.str.2008.08.003
    [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. doi: 10.1073/pnas.1015739108
    [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. doi: 10.1016/j.virol.2012.01.040
    [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. doi: 10.1073/pnas.1407020111
    [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. doi: 10.1073/pnas.0502164102
    [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. doi: 10.1038/73347
    [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. doi: 10.1073/pnas.1309947110
    [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. doi: 10.1007/s10858-005-0945-7
    [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. doi: 10.1016/j.molcel.2005.03.013
    [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. doi: 10.1126/science.7997879
    [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. doi: 10.1128/JVI.01509-14
    [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. doi: 10.1007/s13238-013-3060-7
    [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. doi: 10.1016/j.virol.2011.06.019
    [32] Bujnicki JM (2002) Sequence permutations in the molecular evolution of DNA methyltransferases. BMC Evol Biol 2: 3. doi: 10.1186/1471-2148-2-3
    [33] Peisajovich SG, Rockah L, Tawfik DS (2006) Evolution of new protein topologies through multistep gene rearrangements. Nat Genet 38: 168-174. doi: 10.1038/ng1717
    [34] Vogel C, Morea V (2006) Duplication, divergence and formation of novel protein topologies. Bio Essays 28: 973-978.
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