CoChat
Sign Up
PreprintCited by 10Viral Infectious Diseases and Gene Expression in InsectsAdvanced Electron Microscopy Techniques and ApplicationsEnzyme Structure and Function

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Helical reconstruction of VP39 reveals principles for baculovirus nucleocapsid assembly

Open access
Benning, Friederike M. C., Jenni, Simon, Garcia, Coby Y., Nguyen, Tran H., Zhang, Xuewu, Chao, Luke H.·2023·Nature Communications
DOI 10.1101/2023.06.15.545104PMC PMC10767040

Preprint — published as 10.1038/s41467-023-44596-y

Open this paper in CoChat — free accountOpen PDF

Abstract

Baculoviruses are insect-infecting pathogens with wide applications as biological pesticides, in vitro protein production vehicles and gene therapy tools. Its cylindrical nucleocapsid, which encapsulates and protects the circular double-stranded viral DNA encoding proteins for viral replication and entry, is formed by the highly conserved major capsid protein VP39. The mechanism for VP39 assembly remains unknown. We determined a 3.2 Å electron cryomicroscopy helical reconstruction of an infectious nucleocapsid of Autographa californica multiple nucleopolyhedrovirus, revealing how dimers of VP39 assemble into a 14-stranded helical tube. We show that VP39 comprises a unique protein fold conserved across baculoviruses, which includes a Zinc finger domain and a stabilizing intra-dimer sling. Analysis of sample polymorphism revealed that VP39 assembles in several closely-related helical geometries. This VP39 reconstruction reveals general principles for baculoviral nucleocapsid assembly.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1101/2023.06.15.545104

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 94

  1. Landwehr, A . Benefits of Baculovirus Use in IPM Strategies for Open Field and Protected Vegetables. Frontiers in Sustainable Food Systems 4(2021). · DOI
  2. 2021, Climate warming promotes pesticide resistance through expanding overwintering range of a global pest, Nature Communications, 12, 5351, 10.1038/s41467-021-25505-7 · DOI
  3. 10.1158/0008-5472.CAN-05-4514 · DOI
  4. 10.3748/wjg.14.5810 · DOI
  5. 10.1038/mt.2009.22 · DOI
  6. Ono, C. , Okamoto, T. , Abe, T. & Matsuura, Y . Baculovirus as a Tool for Gene Delivery and Gene Therapy. Viruses 10, 510 (2018). · DOI
  7. Garcia Fallit, M. , et al. Evaluation of Baculoviruses as Gene Therapy Vectors for Brain Cancer. Viruses 15, 608 (2023). · DOI
  8. Hong, M. et al. Genetic engineering of baculovirus-insect cell system to improve protein production. Frontiers in Bioengineering and Biotechnology 10(2022). · DOI
  9. Pidre, M.L. , Arrías, P.N. , Amorós Morales, L.C. & Romanowski, V . The Magic Staff: A Comprehensive Overview of Baculovirus-Based Technologies Applied to Human and Animal Health. Viruses 15, 80 (2023). · DOI
  10. 10.1007/s00705-006-0763-6 · DOI
  11. 10.1006/jipa.1993.1090 · DOI
  12. 10.1128/JVI.78.13.7023-7035.2004 · DOI
  13. 10.1006/viro.1999.9894 · DOI
  14. 10.1016/j.jip.2015.12.001 · DOI
  15. 1982, Structure of the baculovirus nucleocapsid, Virology, 120, 433, 10.1016/0042-6822(82)90043-5 · DOI
  16. 2018, Controllable Assembly of Flexible Protein Nanotubes for Loading Multifunctional Modules, ACS Applied Materials & Interfaces, 10, 25135, 10.1021/acsami.8b07611 · DOI
  17. 2018, Baculovirus Entry and Egress from Insect Cells, Annual Review of Virology, 5, 113, 10.1146/annurev-virology-092917-043356 · DOI
  18. 1986, Ultrastructure of baculoviruses, The Biology of Baculoviruses, 1, 61
  19. 1988, p39, a major baculovirus structural protein: Immunocytochemical characterization and genetic location, Virology, 167, 407
  20. 1989, Identification, sequence, and transcriptional mapping of the major capsid protein gene of the baculovirus Autographa californica nuclear polyhedrosis virus, J Virol, 63, 2008, 10.1128/jvi.63.5.2008-2018.1989 · DOI
  21. 10.1016/j.virusres.2012.02.016 · DOI
  22. Bai, H. et al. Major capsid protein of Autographa californica multiple nucleopolyhedrovirus contributes to the promoter activity of the very late viral genes. Virus Research 273, 197758 (2019). · DOI
  23. Katsuma, S. & Kokusho, R . A Conserved Glycine Residue Is Required for Proper Functioning of a Baculovirus VP39 Protein. J Virol 91(2017). · DOI
  24. 10.1038/nsmb.3054 · DOI
  25. 10.1016/0889-1605(86)90040-6 · DOI
  26. Zhao, S. , He, G. , Yang, Y. & Liang, C . Nucleocapsid Assembly of Baculoviruses. Viruses 11(2019). · DOI
  27. 10.1371/journal.ppat.1006823 · DOI
  28. 10.1016/j.jmb.2008.08.063 · DOI
  29. 2014, Revisiting the genome packaging in viruses with lessons from the "Giants", Virology, 466-467, 15, 10.1016/j.virol.2014.06.022 · DOI
  30. Lai, Q. et al. The 38K-Mediated Specific Dephosphorylation of the Viral Core Protein P6.9 Plays an Important Role in the Nucleocapsid Assembly of Autographa californica Multiple Nucleopolyhedrovirus. J Virol 92(2018). · DOI
  31. 2020, Identification of A functional region in Bombyx mori nucleopolyhedrovirus VP39 that is essential for nuclear actin polymerization, Virology, 550, 37, 10.1016/j.virol.2020.06.015 · DOI
  32. 10.1006/viro.1998.9065 · DOI
  33. 10.1128/JVI.06109-11 · DOI
  34. 10.1016/j.virol.2008.12.023 · DOI
  35. 10.1128/JVI.73.10.8559-8570.1999 · DOI
  36. 10.1128/JVI.00948-08 · DOI
  37. 2013, Screening of candidate proteins interacting with IE-2 of Bombyx mori nucleopolyhedrovirus, Molecular Biology Reports, 40, 5797, 10.1007/s11033-013-2683-3 · DOI
  38. 10.1006/viro.1994.1332 · DOI
  39. 10.1128/JVI.01778-08 · DOI
  40. 10.1371/journal.pone.0128471 · DOI
  41. Li, S. et al. VP39 of Spodoptera litura multicapsid nucleopolyhedrovirus cannot efficiently rescue the nucleocapsid assembly of vp39-null Autographa californica multiple nucleopolyhedrovirus. Virology Journal 18, 81 (2021). · DOI
  42. 10.1073/pnas.1919114117 · DOI
  43. 2022, Python-based Helix Indexer: A graphical user interface program for finding symmetry of helical assembly through Fourier-Bessel indexing of electron microscopic data, Protein Sci, 31, 107, 10.1002/pro.4186 · DOI
  44. 10.1016/j.jsb.2017.02.003 · DOI
  45. Jamali, K. et al. Automated model building and protein identification in cryo-EM maps. bioRxiv, 2023.05.16.541002 (2023). · DOI · Paper page
  46. 10.1107/S0907444910007493 · DOI · Paper page
  47. 10.1093/nar/gkac387 · DOI
  48. Kempen, M.v. , et al. Fast and accurate protein structure search with Foldseek. bioRxiv, 2022.02.07.479398 (2023).
  49. 10.1107/S0907444904004081 · DOI
  50. 10.1016/j.jmb.2007.05.022 · DOI
  51. Evans, R. , et al. Protein complex prediction with AlphaFold-Multimer. bioRxiv, 2021.10.04.463034 (2022).
  52. 2022, Visualizing molecular interactions that determine assembly of a bullet-shaped vesicular stomatitis virus particle, Nature Communications, 13, 4802, 10.1038/s41467-022-32223-1 · DOI
  53. 10.7554/eLife.70307 · DOI
  54. 10.1016/j.str.2016.04.015 · DOI
  55. 10.1016/j.str.2006.05.018 · DOI
  56. 10.1016/S0076-6879(10)82006-3 · DOI
  57. 10.1016/j.str.2020.08.010 · DOI
  58. 10.1016/j.cub.2018.05.027 · DOI
  59. 10.1083/jcb.201201120 · DOI
  60. Greenan, G.A. , Vale, R.D. & Agard, D.A . Electron cryotomography of intact motile cilia defines the basal body to axoneme transition. J Cell Biol 219(2020). · DOI
  61. 10.7554/eLife.04969 · DOI
  62. 10.1016/j.pep.2009.01.002 · DOI
  63. 10.1073/pnas.1919114117 · DOI
  64. 10.1038/nmeth.4193 · DOI
  65. 10.1016/j.jsb.2015.08.008 · DOI
  66. 10.1042/BCJ20210708 · DOI
  67. 10.1016/j.jsb.2012.09.006 · DOI · Paper page
  68. 2020, Amyloid structure determination in RELION-3.1, Acta Crystallogr D Struct Biol, 76, 94, 10.1107/S2059798319016577 · DOI
  69. 10.7554/eLife.35383 · DOI
  70. 2017, cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination, Nature Methods, 14, 290, 10.1038/nmeth.4169 · DOI · Paper page
  71. 2020, Non-uniform refinement: adaptive regularization improves single-particle cryo-EM reconstruction, Nature Methods, 17, 1214, 10.1038/s41592-020-00990-8 · DOI
  72. 10.1038/s41586-020-2649-2 · DOI · Paper page
  73. 10.1006/jsbi.1996.0013 · DOI
  74. 2011, A unified convention for biological assemblies with helical symmetry, Acta Crystallogr D Biol Crystallogr, 67, 716, 10.1107/S0907444911024024 · DOI
  75. 2020, SciPy 1.0: fundamental algorithms for scientific computing in Python, Nature Methods, 17, 261, 10.1038/s41592-019-0686-2 · DOI · Paper page
  76. 10.1107/S0907444910045749 · DOI · Paper page
  77. 2018, Real-space refinement in PHENIX for cryo-EM and crystallography, Acta Crystallographica Section D, 74, 531, 10.1107/S2059798318006551 · DOI
  78. 2019, Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix, Acta Crystallographica Section D, 75, 861, 10.1107/S2059798319011471 · DOI · Paper page
  79. 10.1002/pro.3330 · DOI · Paper page
  80. 10.1002/PRO.3943 · DOI
  81. 10.1093/nar/gkab1112 · DOI · Paper page
  82. 10.1006/jmbi.1990.9999 · DOI · Paper page
  83. 2017, MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization, Briefings in Bioinformatics, 20, 1160
  84. 10.1093/nar/gkt389 · DOI
  85. 10.1093/bioinformatics/btp033 · DOI
  86. 10.1093/nar/gki370 · DOI
  87. 10.1002/pro.4582 · DOI
  88. 2022, Search and sequence analysis tools services from EMBL-EBI in 2022, Nucleic acids research, 50, W276, 10.1093/nar/gkac240 · DOI
  89. 10.1093/oxfordjournals.molbev.a040454 · DOI
  90. 10.1093/NAR/GKAB301 · DOI
  91. 10.1038/S41592-022-01488-1 · DOI · Paper page
  92. Cianfrocco, M.A. , Wong-Barnum, M. , Youn, C. , Wagner, R. & Leschziner, A . COSMIC2: A Science Gateway for Cryo-Electron Microscopy Structure Determination. in Proceedings of the Practice and Experience in Advanced Research Computing 2017 on Sustainability , Success and Impact Article 22 (Association for Computing Machinery, New Orleans, LA, USA, 2017). · DOI
  93. 2022, UniProt: the Universal Protein Knowledgebase in 2023, Nucleic Acids Research, 51, D523
  94. 10.1093/nar/gkv1189 · DOI · Paper page

Metadata

Authors
Benning, F. M. C., Jenni, S., Garcia, C. Y., Nguyen, T. H., Zhang, X., & Chao, L. H.
Affiliations
  • Harvard University (US)
  • Massachusetts General Hospital (US)
  • The University of Texas Southwestern Medical Center (US)
Corresponding author
Chao, Luke H.
ORCID
Venue
Nature Communications
Publisher
openRxiv
Published
2023-06-15
Volume
15
Issue
1
Pages
250-250
ISSN
2041-1723 (ISSN-L)
DOI
10.1101/2023.06.15.545104
PMC
PMC10767040
OpenAlex
W4390583912
Cited by
10
References
1
Citations by year
2025: 6 · 2024: 3 · 2023: 1
FWCI
1.23
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Science Foundation
  • U.S. Department of Health and Human Services (R35GM130289, R35GM142553)
  • Leona M. and Harry B. Helmsley Charitable Trust
  • Brandeis University
  • York University
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (180777)
  • National Institutes of Health
  • NYU Grossman School of Medicine
  • National Institute of General Medical Sciences (R35GM142553, R35GM130289)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Viral Infectious Diseases and Gene Expression in Insects
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
Keywords
baculovirus, nucleocapsid assembly, VP39, major capsid protein, Autographa californica nuclear polyhedrosis virus, helical reconstruction, zinc finger, protein dimerization, helical tubes

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review