The atomic structure of baculovirus polyhedra reveals the independent emergence of infectious crystals in DNA and RNA viruses

Fasseli Joseph Coulibaly, Elaine Chiu, Sascha Gutmann, Chitra Rajendran, Peter W Haebel, Keiko D Ikeda, Hajime Mori, Vernon K Ward, Clemens Schulze-Briese, Peter Metcalf

Research output: Contribution to journalArticleResearchpeer-review

Abstract

Baculoviruses are ubiquitous insect viruses well known for their use as bioinsecticides, gene therapy vectors, and protein expression systems. Overexpression of recombinant proteins in insect cell culture utilizes the strong promoter of the polyhedrin gene. In infected larvae, the polyhedrin protein forms robust intracellular crystals called polyhedra, which protect encased virions for prolonged periods in the environment. Polyhedra are produced by two unrelated families of insect viruses, baculoviruses and cypoviruses. The atomic structure of cypovirus polyhedra revealed an intricate packing of trimers, which are interconnected by a projecting N-terminal helical arm of the polyhedrin molecule. Baculovirus and cypovirus polyhedra share nearly identical lattices, and the N-terminal region of the otherwise unrelated baculovirus polyhedrin protein sequence is also predicted to be alpha-helical. These results suggest homology between the proteins and a common structural basis for viral polyhedra. Here, we present the 2.2-A structure of baculovirus polyhedra determined by x-ray crystallography from microcrystals produced in vivo. We show that the underlying molecular organization is, in fact, very different. Although both polyhedra have nearly identical unit cell dimensions and share I23 symmetry, the polyhedrin molecules are structurally unrelated and pack differently in the crystals. In particular, disulfide bonds and domain-swapped N-terminal domains stabilize the building blocks of baculovirus polyhedra and interlocking C-terminal arms join unit cells together. We show that the N-terminal projecting helical arms have different structural roles in baculovirus and cypovirus polyhedra and conclude that there is no structural evidence for a common evolutionary origin for both classes of polyhedra.
Original languageEnglish
Pages (from-to)22205 - 22210
Number of pages6
JournalProceedings of the National Academy of Sciences
Volume106
Issue number52
DOIs
Publication statusPublished - 2009

Cite this

Coulibaly, Fasseli Joseph ; Chiu, Elaine ; Gutmann, Sascha ; Rajendran, Chitra ; Haebel, Peter W ; Ikeda, Keiko D ; Mori, Hajime ; Ward, Vernon K ; Schulze-Briese, Clemens ; Metcalf, Peter. / The atomic structure of baculovirus polyhedra reveals the independent emergence of infectious crystals in DNA and RNA viruses. In: Proceedings of the National Academy of Sciences. 2009 ; Vol. 106, No. 52. pp. 22205 - 22210.
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title = "The atomic structure of baculovirus polyhedra reveals the independent emergence of infectious crystals in DNA and RNA viruses",
abstract = "Baculoviruses are ubiquitous insect viruses well known for their use as bioinsecticides, gene therapy vectors, and protein expression systems. Overexpression of recombinant proteins in insect cell culture utilizes the strong promoter of the polyhedrin gene. In infected larvae, the polyhedrin protein forms robust intracellular crystals called polyhedra, which protect encased virions for prolonged periods in the environment. Polyhedra are produced by two unrelated families of insect viruses, baculoviruses and cypoviruses. The atomic structure of cypovirus polyhedra revealed an intricate packing of trimers, which are interconnected by a projecting N-terminal helical arm of the polyhedrin molecule. Baculovirus and cypovirus polyhedra share nearly identical lattices, and the N-terminal region of the otherwise unrelated baculovirus polyhedrin protein sequence is also predicted to be alpha-helical. These results suggest homology between the proteins and a common structural basis for viral polyhedra. Here, we present the 2.2-A structure of baculovirus polyhedra determined by x-ray crystallography from microcrystals produced in vivo. We show that the underlying molecular organization is, in fact, very different. Although both polyhedra have nearly identical unit cell dimensions and share I23 symmetry, the polyhedrin molecules are structurally unrelated and pack differently in the crystals. In particular, disulfide bonds and domain-swapped N-terminal domains stabilize the building blocks of baculovirus polyhedra and interlocking C-terminal arms join unit cells together. We show that the N-terminal projecting helical arms have different structural roles in baculovirus and cypovirus polyhedra and conclude that there is no structural evidence for a common evolutionary origin for both classes of polyhedra.",
author = "Coulibaly, {Fasseli Joseph} and Elaine Chiu and Sascha Gutmann and Chitra Rajendran and Haebel, {Peter W} and Ikeda, {Keiko D} and Hajime Mori and Ward, {Vernon K} and Clemens Schulze-Briese and Peter Metcalf",
year = "2009",
doi = "10.1073/pnas.0910686106",
language = "English",
volume = "106",
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Coulibaly, FJ, Chiu, E, Gutmann, S, Rajendran, C, Haebel, PW, Ikeda, KD, Mori, H, Ward, VK, Schulze-Briese, C & Metcalf, P 2009, 'The atomic structure of baculovirus polyhedra reveals the independent emergence of infectious crystals in DNA and RNA viruses' Proceedings of the National Academy of Sciences, vol. 106, no. 52, pp. 22205 - 22210. https://doi.org/10.1073/pnas.0910686106

The atomic structure of baculovirus polyhedra reveals the independent emergence of infectious crystals in DNA and RNA viruses. / Coulibaly, Fasseli Joseph; Chiu, Elaine; Gutmann, Sascha; Rajendran, Chitra; Haebel, Peter W; Ikeda, Keiko D; Mori, Hajime; Ward, Vernon K; Schulze-Briese, Clemens; Metcalf, Peter.

In: Proceedings of the National Academy of Sciences, Vol. 106, No. 52, 2009, p. 22205 - 22210.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - The atomic structure of baculovirus polyhedra reveals the independent emergence of infectious crystals in DNA and RNA viruses

AU - Coulibaly, Fasseli Joseph

AU - Chiu, Elaine

AU - Gutmann, Sascha

AU - Rajendran, Chitra

AU - Haebel, Peter W

AU - Ikeda, Keiko D

AU - Mori, Hajime

AU - Ward, Vernon K

AU - Schulze-Briese, Clemens

AU - Metcalf, Peter

PY - 2009

Y1 - 2009

N2 - Baculoviruses are ubiquitous insect viruses well known for their use as bioinsecticides, gene therapy vectors, and protein expression systems. Overexpression of recombinant proteins in insect cell culture utilizes the strong promoter of the polyhedrin gene. In infected larvae, the polyhedrin protein forms robust intracellular crystals called polyhedra, which protect encased virions for prolonged periods in the environment. Polyhedra are produced by two unrelated families of insect viruses, baculoviruses and cypoviruses. The atomic structure of cypovirus polyhedra revealed an intricate packing of trimers, which are interconnected by a projecting N-terminal helical arm of the polyhedrin molecule. Baculovirus and cypovirus polyhedra share nearly identical lattices, and the N-terminal region of the otherwise unrelated baculovirus polyhedrin protein sequence is also predicted to be alpha-helical. These results suggest homology between the proteins and a common structural basis for viral polyhedra. Here, we present the 2.2-A structure of baculovirus polyhedra determined by x-ray crystallography from microcrystals produced in vivo. We show that the underlying molecular organization is, in fact, very different. Although both polyhedra have nearly identical unit cell dimensions and share I23 symmetry, the polyhedrin molecules are structurally unrelated and pack differently in the crystals. In particular, disulfide bonds and domain-swapped N-terminal domains stabilize the building blocks of baculovirus polyhedra and interlocking C-terminal arms join unit cells together. We show that the N-terminal projecting helical arms have different structural roles in baculovirus and cypovirus polyhedra and conclude that there is no structural evidence for a common evolutionary origin for both classes of polyhedra.

AB - Baculoviruses are ubiquitous insect viruses well known for their use as bioinsecticides, gene therapy vectors, and protein expression systems. Overexpression of recombinant proteins in insect cell culture utilizes the strong promoter of the polyhedrin gene. In infected larvae, the polyhedrin protein forms robust intracellular crystals called polyhedra, which protect encased virions for prolonged periods in the environment. Polyhedra are produced by two unrelated families of insect viruses, baculoviruses and cypoviruses. The atomic structure of cypovirus polyhedra revealed an intricate packing of trimers, which are interconnected by a projecting N-terminal helical arm of the polyhedrin molecule. Baculovirus and cypovirus polyhedra share nearly identical lattices, and the N-terminal region of the otherwise unrelated baculovirus polyhedrin protein sequence is also predicted to be alpha-helical. These results suggest homology between the proteins and a common structural basis for viral polyhedra. Here, we present the 2.2-A structure of baculovirus polyhedra determined by x-ray crystallography from microcrystals produced in vivo. We show that the underlying molecular organization is, in fact, very different. Although both polyhedra have nearly identical unit cell dimensions and share I23 symmetry, the polyhedrin molecules are structurally unrelated and pack differently in the crystals. In particular, disulfide bonds and domain-swapped N-terminal domains stabilize the building blocks of baculovirus polyhedra and interlocking C-terminal arms join unit cells together. We show that the N-terminal projecting helical arms have different structural roles in baculovirus and cypovirus polyhedra and conclude that there is no structural evidence for a common evolutionary origin for both classes of polyhedra.

UR - http://www.pnas.org/content/106/52/22205.full.pdf

U2 - 10.1073/pnas.0910686106

DO - 10.1073/pnas.0910686106

M3 - Article

VL - 106

SP - 22205

EP - 22210

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 52

ER -