Crystal Structures of a Piscine Betanodavirus: Mechanisms of Capsid Assembly and Viral Infection

1. Ahlquist P. RNA-dependent RNA polymerases, viruses, and RNA silencing. Science. 2002;296 : 1270–1273. 12016304

2. Ahlquist P. Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat Rev Microbiol. 2005;4 : 371–382.

3. Chao JA, Lee JH, Chapados BR, Debler EW, Schneemann A, Williamson JR. Dual modes of RNA-silencing suppression by Flock house virus protein B2. Nat Struct Mol Biol. 2006;12 : 952–957.

4. Li Y, Lu JF, Han YH, Fan XX, Ding SW. RNA interference functions as an antiviral immunity mechanism in mammals. Science. 2013;342 : 231–234. doi: 10.1126/science.1241911 24115437

5. Lu R, Maduro M, Li F, Li HW, Broitman-Maduro G, Li WX, et al. Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature. 2005;436 : 1040–1043. 16107851

6. Ou MC, Chen YM, Jeng MF, Chu CJ, Yang HL, Chen TY. Identification of critical residues in nervous necrosis virus B2 for dsRNA-binding and RNAi-inhibiting activity through by bioinformatic analysis and mutagenesis. Biochem Bioph Res Co. 2007;361 : 634–640.

7. Thiery R, Cozien J, de Boisseson C, Kerbart-Boscher S, Nevarez L. Genomic classification of new betanodavirus isolates by phylogenetic analysis of the coat protein gene suggests a low host-fish species specificity. J Gen Virol. 2004;85 : 3079–3087. 15448371

8. Yoshikoshi K, Inoue K. Viral nervous necrosis in hatchery-reared larvae and juveniles of Japanese parrotfish, Oplegnathus fasciatus (Temminck and Schlegel). J Fish Dis. 1990;13 : 69–77.

9. Munday BL, Kwang J, Moody N. Betanodavirus infections of teleost fish: a review. J Fish Dis. 2002;25 : 127–142.

10. Nishizawa T, Furuhashi M, Nagai T, Nakai T, Muroga K. Genomic classification of fish nodaviruses by molecular phylogenetic analysis of the coat protein gene. Appl Environ Microb. 1997;63 : 1633–1636.

11. Schuster S, Zirkel F, Kurth A, van Cleef KWR, Drosten C, van Rij RP, et al. A unique nodavirus with novel features: mosinovirus expresses two subgenomic RNAs, a capsid gene of unknown origin, and a suppressor of the antiviral RNA interference pathway. J Virol. 2014;88 : 13447–13459. doi: 10.1128/JVI.02144-14 25210176

12. Tang KF, Pantoja CR, Redman RM, Navarro SA, Lightner DV. Ultrastructural and sequence characterization of Penaeus vannamei nodavirus (PvNV) from Belize. Dis Aquat Organ. 2011;94 : 179–187 doi: 10.3354/dao02335 21790065

13. Cheng SS, Brooks CL. Viral capsid proteins are segregated in structural fold space. PLoS Comput Biol. 2013;9: e1002905. doi: 10.1371/journal.pcbi.1002905 23408879

14. Schneemann A, Zhong WD, Gallagher TM, Rueckert RR. Maturation cleavage required for infectivity of a nodavirus. J Virol. 1992;66 : 6728–6734. 1404613

15. Tang L, Johnson KN, Ball LA, Lin TW, Yeager M, Johnson JE. The structure of Pariacoto virus reveals a dodecahedral cage of duplex RNA. Nat Struct Biol. 2001;8 : 77–83. 11135676

16. Fisher AJ, Johnson JE. Ordered duplex RNA controls capsid architecture in an icosahedral animal virus. Nature. 1993;361 : 176–179. 8421524

17. Dong XF, Natarajan P, Tihova M, Johnson JE, Schneemann A. Particle polymorphism caused by deletion of a peptide molecular switch in a quasi-equivalent icosahedral virus. J Virol. 1998;72 : 6024–6033. 9621065

18. Tang L, Lin CS, Krishna NK, Yeager M, Schneemann A, Johnson JE. Virus-like particles of a fish nodavirus display a capsid subunit domain organization different from that of insect nodaviruses. J Virol. 2002;76 : 6370–6375. 12021370

19. Qu CX, Liljas L, Opalka N, Brugidou C, Yeager M, Beachy RN, et al. 3D domain swapping modulates the stability of members of an icosahedral virus group. Structure. 2000;8 : 1095–1103. 11080631

20. Pappachan A, Subashchandrabose C, Satheshkumar PS, Savithri HS, Murthy MRN. Structure of recombinant capsids formed by the beta-annulus deletion mutant–rCP (Delta 48–59) of Sesbania mosaic virus. Virology. 2008;375 : 190–196. doi: 10.1016/j.virol.2008.01.023 18295296

21. Satheshkumar PS, Lokesh GL, Murthy MRN, Savithri HS. The role of arginine-rich motif and beta-annulus in the assembly and stability of Sesbania mosaic virus capsids. J Mol Biol. 2005;353 : 447–458. 16169007

22. Chen R, Neill JD, Estes MK, Prasad BVV. X-ray structure of a native calicivirus: structural insights into antigenic diversity and host specificity. Proc Natl Acad Sci USA. 2006;103 : 8048–8053. 16702551

23. Holm L, Sander C. Dali: a network tool for protein-structure comparison. Trends Biochem Sci. 1995;20 : 478–480. 8578593

24. Guo YR, Hryc CF, Jakana J, Jiang H, Wang D, Chiu W, et al. Crystal structure of a nematode-infecting virus. Proc Natl Acad Sci USA. 2014;111 : 12781–12786. doi: 10.1073/pnas.1407122111 25136116

25. Morgunova EY, Dauter Z, Fry E, Stuart DI, Stelmashchuk VY, Mikhailov AM, et al. The atomic-structure of Carnation Mottle Virus capsid protein. Febs Lett. 1994;338 : 267–271. 8307192

26. Prasad BVV, Schmid MF. Principles of virus structural organization. Adv Exp Med Biol. 2012;726 : 17–47. doi: 10.1007/978-1-4614-0980-9_3 22297509

27. Banerjee M, Speir JA, Kwan MH, Huang R, Aryanpur PP, Bothner B, et al. Structure and function of a genetically engineered mimic of a nonenveloped virus entry intermediate. J Virol. 2010;84 : 4737–4746. doi: 10.1128/JVI.02670-09 20164221

28. Li M, Kakani K, Katpally U, Johnson S, Rochon D, Smith TJ. Atomic structure of Cucumber necrosis virus and the role of the capsid in vector transmission. J Virol. 2013;87 : 12166–12175. doi: 10.1128/JVI.01965-13 24006433

29. Harrison SC, Olson AJ, Schutt CE, Winkler FK, Bricogne G. Tomato bushy stunt virus at 2.9-a resolution. Nature. 1978;276 : 368–373. 19711552

30. Hogle J, Kirchhausen T, Harrison SC. Divalent-cation sites in tomato bushy stunt virus—difference maps at 2.9 Å resolution. J Mol Biol. 1983;171 : 95–100. 6417343

31. Satheshkumar PS, Lokesh GL, Sangita V, Saravanan V, Vijay CS, Murthy MRN, et al. Role of metal ion-mediated interactions in the assembly and stability of Sesbania mosaic virus T = 3 and T = 1 capsids. J Mol Biol. 2004;342 : 1001–1014. 15342252

32. Wery JP, Reddy VS, Hosur MV, Johnson JE. The refined three-dimensional structure of an insect virus at 2.8 Å resolution. J Mol Biol. 1994;235 : 565–586. 8289282

33. Guu TSY, Liu Z, Ye QZ, Mata DA, Li KP, Yin CC, et al. Structure of the hepatitis E virus-like particle suggests mechanisms for virus assembly and receptor binding. Proc Natl Acad Sci USA. 2009;106 : 12992–12997. doi: 10.1073/pnas.0904848106 19622744

34. Yamashita T, Mori Y, Miyazaki N, Cheng RH, Yoshimura M, Unno H, et al. Biological and immunological characteristics of hepatitis E virus-like particles based on the crystal structure. Proc Natl Acad Sci USA. 2009;106 : 12986–12991. doi: 10.1073/pnas.0903699106 19620712

35. Sangita V, Satheshkumar PS, Savithri HS, Murthy MRN. Structure of a mutant T = 1 capsid of Sesbania mosaic virus: role of water molecules in capsid architecture and integrity. Acta Crystallogr D Biol Crystallogr. 2005;61 : 1406–1412. 16204894

36. Schulze A, Gripon P, Urban S. Hepatitis B virus infection initiates with a large surface protein-dependent binding to heparan sulfate proteoglycans. Hepatology. 2007;46 : 1759–1768. 18046710

37. Schneemann A. The structural and functional role of RNA in icosahedral virus assembly. Annu Rev Microbiol. 2006;60 : 51–67. 16704342

38. Sangita V, Lokesh GL, Satheshkumar PS, Vijay CS, Saravanan V, Savithri HS, et al. T = 1 capsid structures of Sesbania mosaic virus coat protein mutants: determinants of T = 3 and T = 1 capsid assembly. J Mol Biol. 2004;342 : 1402–1405.

39. Abadzapatero C, Abdelmeguid SS, Johnson JE, Leslie AGW, Rayment I, Rossmann MG, et al. Structure of southern bean mosaic virus at 2.8 Å resolution. Nature. 1980;286 : 33–39. 19711553

40. Silva AM, Rossmann MG. Refined structure of southern bean mosaic-virus at 2.9 Å resolution. J Mol Biol. 1987;197 : 69–87. 3681993

41. Neu U, Khan ZM, Schuch B, Palma AS, Liu Y, Pawlita M, et al. Structures of B-lymphotropic polyomavirus VP1 in complex with oligosaccharide ligands. PLoS Pathog. 2013;9: e1003714. doi: 10.1371/journal.ppat.1003714 24204265

42. Mathieu M, Petitpas I, Navaza J, Lepault J, Kohli E, Pothier P, et al. Atomic structure of the major capsid protein of rotavirus: implications for the architecture of the virion. EMBO J. 2001;20 : 1485–1497. 11285213

43. Wu YM, Hsu CH, Wang CH, Liu WT, Chang WH, Lin CS. Role of the DxxDxD motif in the assembly and stability of betanodavirus particles. Arch Virol. 2008;53 : 1633–1642.

44. Chelvanayagam G, Heringa J, Argos P. Anatomy and evolution of proteins displaying the viral capsid jellyroll topology. J Mol Biol 1992;228 : 220–242. 1447783

45. Wang CH, Hsu CH, Wu YM, Luo YC, Tu MH, Chang WH, et al. Roles of cysteines Cys115 and Cys201 in the assembly and thermostability of grouper betanodavirus particles. Virus Genes. 2010;41 : 73–80. doi: 10.1007/s11262-010-0488-1 20446029

46. Sangita V, Lokesh GL, Satheshkumar PS, Saravanan V, Vijay CS, Savithri HS, et al. Structural studies on recombinant T = 3 capsids of Sesbania mosaic virus coat protein mutants. Acta Crystallogr D Biol Crystallogr. 2005;61 : 1402–1405. 16204893

47. Coulibaly F, Chevalier C, Gutsche I, Pous J, Navaza J, Bressanelli S, et al. The birnavirus crystal structure reveals structural relationships among icosahedral viruses. Cell. 2005;120 : 761–772. 15797378

48. Ito Y, Okinaka Y, Mori KI, Sugaya T, Nishioka T, Oka M, et al. Variable region of betanodavirus RNA2 is sufficient to determine host specificity. Dis Aquat Organ. 2008;79 : 199–205. doi: 10.3354/dao01906 18589996

49. Choi YR, Kim HJ, Lee JY, Kang HA, Kim HJ. Chromatographically-purified capsid proteins of red-spotted grouper nervous necrosis virus expressed in Saccharomyces cerevisiae form virus-like particles. Protein Expres Purif. 2013;89 : 162–168.

50. Tsai B. Penetration of nonenveloped viruses into the cytoplasm. Annu Rev Cell Dev Biol. 2007;23 : 23–43. 17456018

51. Bancroft JB. The self-assembly of spherical plant viruses. Adv Virus Res. 1970;16 : 99–134. 4924992

52. Speir JA, Munshi S, Wang GJ, Baker TS, Johnson JE. Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X-ray crystallography and cryo-electron microscopy. Structure. 1995;3 : 63–78. 7743132

53. Tang JH, Johnson JM, Dryden KA, Young MJ, Zlotnick A, Johnson JE. The role of subunit hinges and molecular "switches" in the control of viral capsid polymorphism. J Struct Biol. 2006;154 : 59–67. 16495083

54. Lee CD, Sun HC, Hu SM, Chiu CF, Homhuan A, Liang SM, et al. An improved SUMO fusion protein system for effective production of native proteins. Protein Sci. 2008;17 : 1241–1248. doi: 10.1110/ps.035188.108 18467498

55. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol. 1997;276 : 307–326.

56. Taka J, Naitow H, Yoshimura M, Miyazaki N, Nakagawa A, Tsukihara T. Ab initio crystal structure determination of spherical viruses that exhibit a centrosymmetric location in the unit cell. Acta Crystallogr D Biol Crystallogr. 2005;61 : 1099–1106. 16041075

57. Vagin A, Teplyakov A. Molecular replacement with MOLREP. Acta Crystallogr D Biol Crystallogr. 2010;66 : 22–25. doi: 10.1107/S0907444909042589 20057045

58. Rayment I. Molecular replacement method at low resolution: optimum strategy and intrinsic limitations as determined by calculations on icosahedral virus models. Acta Crystallogr A. 1983;39 : 102–116.

59. Kleywegt GJ, Jones TA. Software for handling macromolecular envelopes. Acta Crystallogr D Biol Crystallogr. 1999;55 : 941–944. 10089342

60. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, et al. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr. 2011;67 : 235–242. doi: 10.1107/S0907444910045749 21460441

61. Cowtan K. Dm: An automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography. 1994;31 : 34–38.

62. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010;66 : 486–501. doi: 10.1107/S0907444910007493 20383002

63. Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr. 1997;53 : 240–255. 15299926

64. Nicholls RA, Long F, Murshudov GN. Low-resolution refinement tools in REFMAC5. Acta Crystallogr D Biol Crystallogr. 2012;68 : 404–417. doi: 10.1107/S090744491105606X 22505260

65. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, et al. Molprobity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr. 2010;66 : 12–21. doi: 10.1107/S0907444909042073 20057044

66. Stein PE, Boodhoo A, Armstrong GD, Cockle SA, Klein MH, Read RJ. The crystal-structure of pertussis toxin. Structure. 1994;2 : 45–57. 8075982

67. Langer G, Cohen SX, Lamzin VS, Perrakis A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc. 2008;3 : 1171–1179. doi: 10.1038/nprot.2008.91 18600222

68. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010;66 : 213–221. doi: 10.1107/S0907444909052925 20124702

69. Mccoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr. 2007;40 : 658–674. 19461840

70. Chi SC, Hu WW, Lo BJ. Establishment and characterization of a continuous cell line (GF-1) derived from grouper, Epinephelus coioides (Hamilton): a cell line susceptible to grouper nervous necrosis virus (GNNV). J Fish Dis. 1999;22 : 173–182.

71. Kuo HC, Wang TY, Chen PP, Chen YM, Chuang HC, Chen TY. Real-time quantitative pcr assay for monitoring of nervous necrosis virus infection in grouper aquaculture. J Clin Microbiol. 2011;49 : 1090–1096. doi: 10.1128/JCM.01016-10 21233077

72. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28 : 2731–2739. doi: 10.1093/molbev/msr121 21546353