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Fine-Tuning Translation Kinetics Selection as the Driving Force of Codon Usage Bias in the Hepatitis A Virus Capsid


Hepatitis A virus (HAV), the prototype of genus Hepatovirus, has several unique biological characteristics that distinguish it from other members of the Picornaviridae family. Among these, the need for an intact eIF4G factor for the initiation of translation results in an inability to shut down host protein synthesis by a mechanism similar to that of other picornaviruses. Consequently, HAV must inefficiently compete for the cellular translational machinery and this may explain its poor growth in cell culture. In this context of virus/cell competition, HAV has strategically adopted a naturally highly deoptimized codon usage with respect to that of its cellular host. With the aim to optimize its codon usage the virus was adapted to propagate in cells with impaired protein synthesis, in order to make tRNA pools more available for the virus. A significant loss of fitness was the immediate response to the adaptation process that was, however, later on recovered and more associated to a re-deoptimization rather than to an optimization of the codon usage specifically in the capsid coding region. These results exclude translation selection and instead suggest fine-tuning translation kinetics selection as the underlying mechanism of the codon usage bias in this specific genome region. Additionally, the results provide clear evidence of the Red Queen dynamics of evolution since the virus has very much evolved to re-adapt its codon usage to the environmental cellular changing conditions in order to recover the original fitness.


Vyšlo v časopise: Fine-Tuning Translation Kinetics Selection as the Driving Force of Codon Usage Bias in the Hepatitis A Virus Capsid. PLoS Pathog 6(3): e32767. doi:10.1371/journal.ppat.1000797
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000797

Souhrn

Hepatitis A virus (HAV), the prototype of genus Hepatovirus, has several unique biological characteristics that distinguish it from other members of the Picornaviridae family. Among these, the need for an intact eIF4G factor for the initiation of translation results in an inability to shut down host protein synthesis by a mechanism similar to that of other picornaviruses. Consequently, HAV must inefficiently compete for the cellular translational machinery and this may explain its poor growth in cell culture. In this context of virus/cell competition, HAV has strategically adopted a naturally highly deoptimized codon usage with respect to that of its cellular host. With the aim to optimize its codon usage the virus was adapted to propagate in cells with impaired protein synthesis, in order to make tRNA pools more available for the virus. A significant loss of fitness was the immediate response to the adaptation process that was, however, later on recovered and more associated to a re-deoptimization rather than to an optimization of the codon usage specifically in the capsid coding region. These results exclude translation selection and instead suggest fine-tuning translation kinetics selection as the underlying mechanism of the codon usage bias in this specific genome region. Additionally, the results provide clear evidence of the Red Queen dynamics of evolution since the virus has very much evolved to re-adapt its codon usage to the environmental cellular changing conditions in order to recover the original fitness.


Zdroje

1. GranthamR

GautierC

GouyM

MercierR

PaveA

1980 Codon catalog usage and the genome hypothesis. Nucl Acids Res 8 197 19c

2. GranthamR

GautierC

GouyM

1980 Codon frequencies in 119 individual genes confirm corsistent choices of degenerate bases according to genome type. Nucl Acids Res 8 1893 1912

3. IkemuraT

1981 Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J Mol Biol 146 1 21

4. BennetzenJL

HallBD

1982 Codon selection in yeast. J Biol Chem 257 3026 3031

5. MoriyamaEN

PowellJR

1997 Codon Usage Bias and tRNA Abundance in Drosophila. J Mol Evol 45 514 523

6. StenicoM

LloydAT

SharpPM

1994 Codon usage in Caenorhabditis elegans: delineation of translational selection and mutational biases. Nucl Acids Res 22 2437 2446

7. ChiapelloH

LisacekF

CabocheM

AlainH

1998 Codon usage and gene function are related in sequences of Arabidopsis thaliana. Gene 209 GC1 GC38

8. MustoH

CruveillerS

D'OnofrioG

RomeroH

BernardiG

2001 Translational Selection on Codon Usage in Xenopus laevis. Mol Biol Evol 18 1703 1707

9. UrrutiaAO

HurstLD

2001 Codon Usage Bias Covaries With Expression Breadth and the Rate of Synonymous Evolution in Humans, but This Is Not Evidence for Selection. Genetics 159 1191 1199

10. SemonM

LobryJR

DuretL

2006 No Evidence for Tissue-Specific Adaptation of Synonymous Codon Usage in Humans. Mol Biol Evol 23 523 529

11. ChamaryJV

HurstL

2005 Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals. Genome Biol 6 R75

12. ChamaryJV

HurstLD

2005 Biased codon usage near intron-exon junctions: selection on splicing enhancers, splice-site recognition or something else? Trends Genet 21 256 259

13. ParmleyJL

ChamaryJV

HurstLD

2006 Evidence for Purifying Selection Against Synonymous Mutations in Mammalian Exonic Splicing Enhancers. Mol Biol Evol 23 301 309

14. PlotkinJB

RobinsH

LevineAJ

2004 Tissue-specific codon usage and the expression of human genes. Proc Natl Acad Sci USA 101 12588 12591

15. LavnerY

KotlarD

2005 Codon bias as a factor in regulating expression via translation rate in the human genome. Gene 345 127 138

16. KomarAA

LesnikT

ReissC

1999 Synonymous codon substitutions affect ribosome traffic and protein folding during in vitro translation. FEBS Lett 462 387 391

17. Kimchi-SarfatyC

OhJM

KimIW

SaunaZE

CalcagnoAM

2007 A “Silent” Polymorphism in the MDR1 Gene Changes Substrate Specificity. Science 315 525 528

18. YangZ

NielsenR

2008 Mutation-Selection Models of Codon Substitution and Their Use to Estimate Selective Strengths on Codon Usage. Mol Biol Evol 25 568 579

19. dos ReisM

SavvaR

WernischL

2004 Solving the riddle of codon usage preferences: a test for translational selection. Nucleic Acids Res 32 5036 5044

20. KarlinS

BlaisdellBE

SchachtelGA

1990 Contrasts in codon usage of latent versus productive genes of Epstein-Barr virus: data and hypotheses. J Virol 64 4264 4273

21. ZhouJ

LiuWJ

PengSW

SunXY

FrazerI

1999 Papillomavirus Capsid Protein Expression Level Depends on the Match between Codon Usage and tRNA Availability. J Virol 73 4972 4982

22. BurnsCC

ShawJ

CampagnoliR

JorbaJ

VincentA

2006 Modulation of Poliovirus Replicative Fitness in HeLa Cells by Deoptimization of Synonymous Codon Usage in the Capsid Region. J Virol 80 3259 3272

23. SanchezG

BoschA

PintoRM

2003 Genome variability and capsid structural constraints of hepatitis a virus. J Virol 77 452 9

24. ColemanJR

PapamichailD

SkienaS

FutcherB

WimmerE

2008 Virus Attenuation by Genome-Scale Changes in Codon Pair Bias. Science 320 1784 1787

25. BuchanJR

AucottLS

StansfieldI

2006 tRNA properties help shape codon pair preferences in open reading frames. Nucl Acids Res 34 1015 1027

26. RacanielloVR

2001 Picornaviridae: The viruses and their replication.

FieldsBN

KnipeDM

HowleyPM

GriffinDE

Fields' virology Philadelphia, Pa Lippincott Williams & Wilkins 685 722

27. AliIK

McKendrickL

MorleySJ

JacksonRJ

2001 Activity of the Hepatitis A Virus IRES Requires Association between the Cap-Binding Translation Initiation Factor (eIF4E) and eIF4G. J Virol 75 7854 7863

28. WhetterLE

DaySP

ElroysteinO

BrownEA

LemonSM

1994 Low efficiency of the 5' nontranslated region of hepatitis A virus RNA in directing cap-independent translation in permissive monkey kidney cells. J Virol 68 5253 5263

29. PintoRM

AragonesL

CostafredaMI

RibesE

BoschA

2007 Codon usage and replicative strategies of hepatitis A virus. Virus Res 127 158 163

30. AragonesL

BoschA

PintoRM

2008 Hepatitis A Virus Mutant Spectra under the Selective Pressure of Monoclonal Antibodies: Codon Usage Constraints Limit Capsid Variability. J Virol 82 1688 1700

31. ReichE

FranklinRM

ShatkinAJ

Tatumel

1962 Action of actinomycin D on animal cells and viruses. Proc Natl Acad Sci USA 48 1238 1245

32. DomingoE

MartinV

PeralesC

Grande-PerezA

Garcia-ArriazaJ

2006 Viruses as quasispecies: biological implications. Curr Top Microbiol Immunol 299 51 82

33. SanchezG

BoschA

Gomez-MarianoG

DomingoE

PintoRM

2003 Evidence for quasispecies distributions in the human hepatitis A virus genome. Virology 315 34 42

34. MuellerS

PapamichailD

ColemanJR

SkienaS

WimmerE

2006 Reduction of the Rate of Poliovirus Protein Synthesis through Large-Scale Codon Deoptimization Causes Attenuation of Viral Virulence by Lowering Specific Infectivity. J Virol 80 9687 9696

35. GellerR

VignuzziM

AndinoR

FrydmanJ

2007 Evolutionary constraints on chaperone-mediated folding provide an antiviral approach refractory to development of drug resistance. Genes Dev 21 195 205

36. Ruiz-JaraboCM

AriasA

BaranowskiE

EscarmisC

DomingoE

2000 Memory in Viral Quasispecies. J Virol 74 3543 3547

37. KrakauerDC

JansenVA

2002 Red queen dynamics of protein translation. J Theor Biol 218 97 109

38. de KokJB

RoelofsRW

GiesendorfBA

PenningsJL

WaasET

2004 Normalization of gene expression measurements in tumor tissues: comparison of 13 endogenous control genes. Lab Invest 85 154 159

39. VandesompeleJ

De PreterK

PattynF

PoppeB

Van RoyN

2002 Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3 0034.1 0034.11

40. Ramos-NinoME

ScapoliL

MartinelliM

LandS

MossmanBT

2003 Microarray Analysis and RNA Silencing Link fra-1 to cd44 and c-met Expression in Mesothelioma. Cancer Res 63 3539 3545

41. PfrunderA

GutmannH

BeglingerC

DreweJ

2003 Gene expression of CYP3A4, ABC-transporters (MDR1 and MRP1-MRP5) and hPXR in three different human colon carcinoma cell lines. J Pharm Pharmacol 55 59 66

42. SanchezG

PintoRM

VanaclochaH

BoschA

2002 Molecular characterization of hepatitis a virus isolates from a transcontinental shellfish-borne outbreak. J Clin Microbiol 40 4148 55

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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