Four levels of hierarchical organization, including noncovalent chainmail, brace the mature tumor herpesvirus capsid against pressurization

Z. Hong Zhou, Wong Hoi Hui, Sanket Shah, Jonathan Jih, Christine M. O'Connor, Michael Sherman, Dean H. Kedes, Stan Schein

Research output: Contribution to journalArticle

11 Citations (Scopus)

Abstract

Like many double-stranded DNA viruses, tumor gammaherpesviruses Epstein-Barr virus and Kaposis sarcoma-associated herpesvirus withstand high internal pressure. Bacteriophage HK97 uses covalent chainmail for this purpose, but how this is achieved noncovalently in the much larger gammaherpesvirus capsid is unknown. Our cryoelectron microscopy structure of a gammaherpesvirus capsid reveals a hierarchy of four levels of organization: (1) Within a hexon capsomer, each monomer of the major capsid protein (MCP), 1,378 amino acids and six domains, interacts with its neighboring MCPs at four sites. (2) Neighboring capsomers are linked in pairs by MCP dimerization domains and in groups of three by heterotrimeric triplex proteins. (3) Small (∼280 amino acids) HK97-like domains in MCP monomers alternate with triplex heterotrimers to form a belt that encircles each capsomer. (4) One hundred sixty-two belts concatenate to form noncovalent chainmail. The triplex heterotrimer orchestrates all four levels and likely drives maturation to an angular capsid that can withstand pressurization.

Original languageEnglish (US)
Pages (from-to)1385-1398
Number of pages14
JournalStructure
Volume22
Issue number10
DOIs
StatePublished - Oct 7 2014

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Braces
Capsid
Herpesviridae
Capsid Proteins
Protein Multimerization
Cryoelectron Microscopy
Amino Acids
Human Herpesvirus 8
Neoplasms
DNA Viruses
Human Herpesvirus 4
Bacteriophages
Pressure
DNA
Proteins

ASJC Scopus subject areas

  • Molecular Biology
  • Structural Biology

Cite this

Four levels of hierarchical organization, including noncovalent chainmail, brace the mature tumor herpesvirus capsid against pressurization. / Zhou, Z. Hong; Hui, Wong Hoi; Shah, Sanket; Jih, Jonathan; O'Connor, Christine M.; Sherman, Michael; Kedes, Dean H.; Schein, Stan.

In: Structure, Vol. 22, No. 10, 07.10.2014, p. 1385-1398.

Research output: Contribution to journalArticle

Zhou, Z. Hong ; Hui, Wong Hoi ; Shah, Sanket ; Jih, Jonathan ; O'Connor, Christine M. ; Sherman, Michael ; Kedes, Dean H. ; Schein, Stan. / Four levels of hierarchical organization, including noncovalent chainmail, brace the mature tumor herpesvirus capsid against pressurization. In: Structure. 2014 ; Vol. 22, No. 10. pp. 1385-1398.
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