Viral genome segmentation can result from a trade-off between genetic content and particle stability

PLoS Genetics

Volumn 7, Issue 3, 2011, Pages

  Ojosnegros, Samuel ^a,e   García Arriaza, Juan ^a,b   Escarmís, Cristina ^a   Manrubia, Susanna C ^c   Perales, Celia ^a   Arias, Armando ^a,f   Mateu, Mauricio García ^a   Domingo, Esteban ^a,d  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c INSTITUTO NACIONAL DE TÉCNICA AEROESPACIAL   (Spain)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

^e CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FOOT AND MOUTH DISEASE VIRUS; GENE TRANSFER; GENETIC STABILITY; GENOME ANALYSIS; GENOME SEGMENTATION; GENOME SIZE; MATHEMATICAL MODEL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RNA REPLICATION; RNA SYNTHESIS; VIRION; VIRUS CAPSID; VIRUS GENOME; VIRUS INACTIVATION; VIRUS MUTATION; VIRUS PARTICLE; VIRUS VIRULENCE; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; CELL LINE; COMPUTER SIMULATION; GENETICS; HAMSTER; KINETICS; METABOLISM; MICROBIAL VIABILITY; PATHOGENICITY; REPRODUCTIVE FITNESS; VIRUS REPLICATION;

MIRIDAE; RNA VIRUSES;

RNA; VIRUS PROTEIN; VIRUS RNA;

ANIMALS; CELL LINE; COMPUTER SIMULATION; CRICETINAE; FOOT-AND-MOUTH DISEASE VIRUS; GENETIC FITNESS; GENOME, VIRAL; KINETICS; MICROBIAL VIABILITY; MODELS, BIOLOGICAL; RNA; RNA, VIRAL; VIRAL PROTEINS; VIRION; VIRUS REPLICATION;

EID: 79953795976     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001344     Document Type: Article

References (33)

1. Garcia-Arriaza J, Manrubia SC, Toja M, Domingo E, Escarmis C, (2004) Evolutionary transition toward defective RNAs that are infectious by complementation. J Virol 78: 11678-11685.
2. Garcia-Arriaza J, Ojosnegros S, Davila M, Domingo E, Escarmis C, (2006) Dynamics of mutation and recombination in a replicating population of complementing, defective viral genomes. J Mol Biol 360: 558-572.
3. Nee S, (1987) The evolution of multicompartmental genomes in viruses. J Mol Evol 25: 277-281.
4. Szathmary E, (1992) Natural selection and dynamical coexistence of defective and complementing virus segments. J Theor Biol 157: 383-406.
5. Chao L, (1988) Evolution of sex in RNA viruses. J Theor Biol 133: 99-112.
6. Holmes EC, (2009) The Evolution and Emergence of RNA Viruses; In: Harvey PM, May RM, editors. Oxford Oxford University Press.
7. Escarmis C, Carrillo EC, Ferrer M, Arriaza JF, Lopez N, et al. (1998) Rapid selection in modified BHK-21 cells of a foot-and-mouth disease virus variant showing alterations in cell tropism. J Virol 72: 10171-10179.
8. Barclay W, Li Q, Hutchinson G, Moon D, Richardson A, et al. (1998) Encapsidation studies of poliovirus subgenomic replicons. J Gen Virol 79 (Pt 7): 1725-1734.
9. Mateo R, Luna E, Rincon V, Mateu MG, (2008) Engineering viable foot-and-mouth disease viruses with increased thermostability as a step in the development of improved vaccines. J Virol 82: 12232-12240.
10. Szathmary E, (1992) Viral sex, levels of selection, and the origin of life. J Theor Biol 159: 99-109.
11. Mills DR, Peterson RL, Spiegelman S, (1967) An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule. Proc Natl Acad Sci USA 58: 217-224.
12. Sabo DL, Domingo E, Bandle EF, Flavell RA, Weissmann C, (1977) A guanosine to adenosine transition in the 3′ terminal extracistronic region of bacteriophage Qβ RNA leading to loss of infectivity. J Mol Biol 112: 235-252.
13. Cole CN, Baltimore D, (1973) Defective interfering particles of poliovirus. IV. Mechanisms of enrichment. J Virol 12: 1414-1426.
14. Lundquist RE, Sullivan M, Maizel JV Jr, (1979) Characterization of a new isolate of poliovirus defective interfering particles. Cell 18: 759-769.
15. Nowak MA, May RM, (2000) Virus Dynamics. Mathematical Principles of Immunology and Virology New York Oxford University Press Inc.
16. Matthews BW, (1968) Solvent content of protein crystals. J Mol Biol 33: 491-497.
17. Johnson JE, Rueckert RR, (1997) Packaging and release of the viral genome. In: Chiu W, Burnett RM, Garcea RL, editors. Structural Biology of Viruses New York Oxford University Press pp. 269-287.
18. Escarmis C, Davila M, Charpentier N, Bracho A, Moya A, et al. (1996) Genetic lesions associated with Muller's ratchet in an RNA virus. J Mol Biol 264: 255-267.
19. Diez J, Davila M, Escarmis C, Mateu MG, Dominguez J, et al. (1990) Unique amino acid substitutions in the capsid proteins of foot-and-mouth disease virus from a persistent infection in cell culture. J Virol 64: 5519-5528.
20. Bett AJ, Prevec L, Graham FL, (1993) Packaging capacity and stability of human adenovirus type 5 vectors. J Virol 67: 5911-5921.
21. Gelbart WM, Knobler CM, (2009) Virology. Pressurized viruses. Science 323: 1682-1683.
22. De Paepe M, Taddei F, (2006) Viruses' life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biol 4: e193 doi:10.1371/journal.pbio.0040193.
23. Chirico N, Vianelli A, Belshaw R Why genes overlap in viruses. Proc Biol Sci 277: 3809-3817.
24. Sobrino F, Davila M, Ortin J, Domingo E, (1983) Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology 128: 310-318.
25. Escarmis C, Davila M, Domingo E, (1999) Multiple molecular pathways for fitness recovery of an RNA virus debilitated by operation of Muller's ratchet. J Mol Biol 285: 495-505.
26. Manrubia SC, Garcia-Arriaza J, Escarmís C, Domingo E, (2006) Long-range transport and universality classes in in vitro viral infection spread. Europhysics Letters 74: 547-553.
27. Perales C, Agudo R, Tejero H, Manrubia SC, Domingo E, (2009) Potential benefits of sequential inhibitor-mutagen treatments of RNA virus infections. PLoS Pathog 5: e1000658 doi:10.1371/journal.ppat.1000658.
28. Perales C, Mateo R, Mateu MG, Domingo E, (2007) Insights into RNA virus mutant spectrum and lethal mutagenesis events: replicative interference and complementation by multiple point mutants. J Mol Biol 369: 985-1000.
29. Mateu MG, Martinez MA, Capucci L, Andreu D, Giralt E, et al. (1990) A single amino acid substitution affects multiple overlapping epitopes in the major antigenic site of foot-and-mouth disease virus of serotype C. J Gen Virol 71 (Pt 3): 629-637.
30. Escarmis C, Perales C, Domingo E, (2009) Biological effect of Muller's Ratchet: distant capsid site can affect picornavirus protein processing. J Virol 83: 6748-6756.
31. Maree AF, Keulen W, Boucher CA, De Boer RJ, (2000) Estimating relative fitness in viral competition experiments. J Virol 74: 11067-11072.
32. Holland JJ, de la Torre JC, Clarke DK, Duarte E, (1991) Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J Virol 65: 2960-2967.
33. Mateo R, Luna E, Mateu MG, (2007) Thermostable variants are not generally represented in foot-and-mouth disease virus quasispecies. J Gen Virol 88: 859-864.