Sequential Adaptive Mutations Enhance Efficient Vector Switching by Chikungunya Virus and Its Epidemic Emergence

English version České info

The adaptation of Chikungunya virus (CHIKV) to a new vector, the Aedes albopictus mosquito, is a major factor contributing to its ongoing re-emergence in a series of large-scale epidemics of arthritic disease in many parts of the world since 2004. Although the initial step of CHIKV adaptation to A. albopictus was determined to involve an A226V amino acid substitution in the E1 envelope glycoprotein that first arose in 2005, little attention has been paid to subsequent CHIKV evolution after this adaptive mutation was convergently selected in several geographic locations. To determine whether selection of second-step adaptive mutations in CHIKV or other arthropod-borne viruses occurs in nature, we tested the effect of an additional envelope glycoprotein amino acid change identified in Kerala, India in 2009. This substitution, E2-L210Q, caused a significant increase in the ability of CHIKV to develop a disseminated infection in A. albopictus, but had no effect on CHIKV fitness in the alternative mosquito vector, A. aegypti, or in vertebrate cell lines. Using infectious viruses or virus-like replicon particles expressing the E2-210Q and E2-210L residues, we determined that E2-L210Q acts primarily at the level of infection of A. albopictus midgut epithelial cells. In addition, we observed that the initial adaptive substitution, E1-A226V, had a significantly stronger effect on CHIKV fitness in A. albopictus than E2-L210Q, thus explaining the observed time differences required for selective sweeps of these mutations in nature. These results indicate that the continuous CHIKV circulation in an A. albopictus-human cycle since 2005 has resulted in the selection of an additional, second-step mutation that may facilitate even more efficient virus circulation and persistence in endemic areas, further increasing the risk of more severe and expanded CHIK epidemics.

Vyšlo v časopise: Sequential Adaptive Mutations Enhance Efficient Vector Switching by Chikungunya Virus and Its Epidemic Emergence. PLoS Pathog 7(12): e32767. doi:10.1371/journal.ppat.1002412
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002412

Souhrn

Zdroje

1. DomingoE 2010 Mechanisms of viral emergence. Vet Res 41 38

2. NijhuisMvan MaarseveenNMBoucherCA 2009 Antiviral resistance and impact on viral replication capacity: evolution of viruses under antiviral pressure occurs in three phases. Handb Exp Pharmacol 299 320

3. ParrishCRKawaokaY 2005 The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu Rev Microbiol 59 553 586

4. ZhangCYWeiJFHeSH 2006 Adaptive evolution of the spike gene of SARS coronavirus: changes in positively selected sites in different epidemic groups. BMC Microbiol 6 88

5. BraultACPowersAMOrtizDEstrada-FrancoJGNavarro-LopezR 2004 Venezuelan equine encephalitis emergence: enhanced vector infection from a single amino acid substitution in the envelope glycoprotein. Proc Natl Acad Sci U S A 101 11344 11349

6. TsetsarkinKAVanlandinghamDLMcGeeCEHiggsS 2007 A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog 3 e201

7. AnishchenkoMBowenRAPaesslerSAustgenLGreeneIP 2006 Venezuelan encephalitis emergence mediated by a phylogenetically predicted viral mutation. Proc Natl Acad Sci U S A 103 4994 4999

8. BraultACHuangCYLangevinSAKinneyRMBowenRA 2007 A single positively selected West Nile viral mutation confers increased virogenesis in American crows. Nat Genet 39 1162 1166

9. TsetsarkinKAChenRLealGForresterNHiggsS 2011 Chikungunya virus emergence is constrained in Asia by lineage-specific adaptive landscapes. Proc Natl Acad Sci U S A 108, 7872-7877

10. MavalankarDShastriPRamanP 2007 Chikungunya epidemic in India: a major public-health disaster. Lancet Infect Dis 7 306 307

11. SchwartzOAlbertML 2010 Biology and pathogenesis of chikungunya virus. Nat Rev Microbiol 8 491 500

12. Nvbdcp. gov 2011 Clinically Supected Chikungunya Fever Cases Since 2007. Available: http://www.nvbdcp.gov.in/chik-cd.html. Accessed 30 October 2011

13. Nvbdcp. gov 2006 Chikungunya Fever Situation in the Country during 2006. Available: http://nvbdcp.gov.in/Chikun-cases.html. Accessed 30 October 2011

14. WeaverSCReisenWK 2010 Present and future arboviral threats. Antiviral Res 85 328 345

15. McCraeAWHendersonBEKiryaBGSempalaSD 1971 Chikungunya virus in the Entebbe area of Uganda: isolations and epidemiology. Trans R Soc Trop Med Hyg 65 152 168

16. DialloMThonnonJTraore-LamizanaMFontenilleD 1999 Vectors of Chikungunya virus in Senegal: current data and transmission cycles. Am J Trop Med Hyg 60 281 286

17. WeinbrenMPHaddowAJWilliamsMC 1958 The occurrence of Chikungunya virus in Uganda. I. Isolation from mosquitoes. Trans R Soc Trop Med Hyg 52 253 257

18. JuppPGMcIntoshBM 1988 Chikungunya virus disease. MonathTP The Arboviruses: Epidemiology and Ecology Boca Raton CRC Press 137 157

19. PowersAMLogueCH 2007 Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus. J Gen Virol 88 2363 2377

20. ChevillonCBriantLRenaudFDevauxC 2008 The Chikungunya threat: an ecological and evolutionary perspective. Trends Microbiol 16 80 88

21. InoueSMoritaKMatiasRRTuplanoJVResuelloRR 2003 Distribution of three arbovirus antibodies among monkeys (Macaca fascicularis) in the Philippines. J Med Primatol 32 89 94

22. ApandiYNazniWANoor AzleenZAVythilingamINoorazianMY 2009 The first isolation of chikungunya virus from nonhuman primates in Malaysia. J Gen Mol Virol 1 035 039

23. YergolkarPNTandaleBVArankalleVASathePSSudeepAB 2006 Chikungunya outbreaks caused by African genotype, India. Emerg Infect Dis 12 1580 1583

24. KumarNPJosephRKamarajTJambulingamP 2008 A226V mutation in virus during the 2007 chikungunya outbreak in Kerala, India. J Gen Virol 89 1945 1948

25. EapenARavindranKJDashAP 2010 Breeding potential of Aedes albopictus (Skuse, 1895) in chikungunya affected areas of Kerala, India. Indian J Med Res 132 733 735

26. RaoBB 2010 Larval habitats of Aedes albopictus (Skuse) in rural areas of Calicut, Kerala, India. J Vector Borne Dis 47 175 177

27. NiyasKPAbrahamRUnnikrishnanRNMathewTNairS 2010 Molecular characterization of Chikungunya virus isolates from clinical samples and adult Aedes albopictus mosquitoes emerged from larvae from Kerala, South India. Virol J 7 189

28. SchuffeneckerIItemanIMichaultAMurriSFrangeulL 2006 Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med 3 e263

29. HapuarachchiHCBandaraKBSumanadasaSDHapugodaMDLaiYL 2009 Re-emergence of Chikungunya Virus in Southeast Asia: Virologic Evidence from Sri Lanka and Singapore. J Gen Virol 91 1067 1076

30. de LamballerieXLeroyECharrelRNTtsetsarkinKHiggsS 2008 Chikungunya virus adapts to tiger mosquito via evolutionary convergence: a sign of things to come? Virol J 5 33

31. SamICChanYFChanSYLoongSKChinHK 2009 Chikungunya virus of Asian and Central/East African genotypes in Malaysia. J Clin Virol 46 180 183

32. NgLCTanLKTanCHTanSSHapuarachchiHC 2009 Entomologic and virologic investigation of Chikungunya, Singapore. Emerg Infect Dis 15 1243 1249

33. LiLJoseJXiangYKuhnRJRossmannMG 2010 Structural changes of envelope proteins during alphavirus fusion. Nature 468 705 708

34. KielianMReyFA 2006 Virus membrane-fusion proteins: more than one way to make a hairpin. Nat Rev Microbiol 4 67 76

35. KielianM 2006 Class II virus membrane fusion proteins. Virology 344 38 47

36. VazeilleMMoutaillerSCoudrierDRousseauxCKhunH 2007 Two Chikungunya isolates from the outbreak of La Reunion (Indian Ocean) exhibit different patterns of infection in the mosquito, Aedes albopictus. PLoS One 2 e1168

37. SanthoshSRDashPKParidaMKhanMRaoPV 2009 Appearance of E1: A226V mutant Chikungunya virus in Coastal Karnataka, India during 2008 outbreak. Virol J 6 172

38. KuhnRJ 2007 Togaviridae: The viruses and their replication. KnipeDMHowleyPM Fields' Virology, Fifth Edition New York Lippincott, Williams and Wilkins 1001 1022

39. VossJEVaneyMCDuquerroySVonrheinCGirard-BlancC 2010 Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature 468 709 712

40. MylesKMPierroDJOlsonKE 2003 Deletions in the putative cell receptor-binding domain of Sindbis virus strain MRE16 E2 glycoprotein reduce midgut infectivity in Aedes aegypti. J Virol 77 8872 8881

41. BurnessATPardoeIFaragherSGVratiSDalgarnoL 1988 Genetic stability of Ross River virus during epidemic spread in nonimmune humans. Virology 167 639 643

42. WoodwardTMMillerBRBeatyBJTrentDWRoehrigJT 1991 A single amino acid change in the E2 glycoprotein of Venezuelan equine encephalitis virus affects replication and dissemination in Aedes aegypti mosquitoes. J Gen Virol 72 (Pt 10) 2431 2435

43. WangKSSchmaljohnALKuhnRJStraussJH 1991 Antiidiotypic antibodies as probes for the Sindbis virus receptor. Virology 181 694 702

44. WangKSStraussJH 1991 Use of a lambda gt11 expression library to localize a neutralizing antibody-binding site in glycoprotein E2 of Sindbis virus. J Virol 65 7037 7040

45. HeilMLAlbeeAStraussJHKuhnRJ 2001 An amino acid substitution in the coding region of the E2 glycoprotein adapts Ross River virus to utilize heparan sulfate as an attachment moiety. J Virol 75 6303 6309

46. TsetsarkinKAMcGeeCEVolkSMVanlandinghamDLWeaverSC 2009 Epistatic roles of E2 glycoprotein mutations in adaption of chikungunya virus to Aedes albopictus and Ae. aegypti mosquitoes. PLoS One 4 e6835

47. Kariuki NjengaMNderituLLedermannJPNdiranguALogueCH 2008 Tracking epidemic Chikungunya virus into the Indian Ocean from East Africa. J Gen Virol 89 2754 2760

48. VolkSMChenRTsetsarkinKAAdamsAPGarciaTI 2010 Genome-scale phylogenetic analyses of chikungunya virus reveal independent emergences of recent epidemics and various evolutionary rates. J Virol 84 6497 6504

49. TeshRBGublerDJRosenL 1976 Variation among goegraphic strains of Aedes albopictus in susceptibility to infection with chikungunya virus. Am J Trop Med Hyg 25 326 335

50. KaurPPonniahMMurhekarMVRamachandranVRamachandranR 2008 Chikungunya outbreak, South India, 2006. Emerg Infect Dis 14 1623 1625

51. DwibediBSabatJMahapatraNKarSKKerkettaAS 2011 Rapid spread of chikungunya virus infection in Orissa: India. Indian J Med Res 133 316 321

52. DuttaPKhanSAKhanAMBorahJChowdhuryP 2011 First evidence of chikungunya virus infection in Assam, Northeast India. Trans R Soc Trop Med Hyg 105 355 357

53. BredenbeekPJFrolovIRiceCMSchlesingerS 1993 Sindbis virus expression vectors: packaging of RNA replicons by using defective helper RNAs. J Virol 67 6439 6446

54. BenedictMQLevineRSHawleyWALounibosLP 2007 Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector Borne Zoonotic Dis 7 76 85

55. AngeliniRFinarelliACAngeliniPPoCPetropulacosK 2007 Chikungunya in north-eastern Italy: a summing up of the outbreak. Euro Surveill 12 E071122 071122

56. RezzaGNicolettiLAngeliniRRomiRFinarelliAC 2007 Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370 1840 1846

57. GrandadamMCaroVPlumetSThibergeJMSouaresY 2011 Chikungunya virus, southeastern france. Emerg Infect Dis 17 910 913

58. VazeilleMMoussonLFaillouxAB 2009 Failure to demonstrate experimental vertical transmission of the epidemic strain of Chikungunya virus in Aedes albopictus from La Reunion Island, Indian Ocean. Mem Inst Oswaldo Cruz 104 632 635

59. DelatteHPaupyCDehecqJSThiriaJFaillouxAB 2008 Aedes albopictus, vector of chikungunya and dengue in Reunion: biology and control. Parasite 15 3 13

60. ThavaraUTawatsinAPengsakulTBhakdeenuanPChanamaS 2009 Outbreak of chikungunya fever in Thailand and virus detection in field population of vector mosquitoes, Aedes aegypti (L.) and Aedes albopictus Skuse (Diptera: Culicidae). Southeast Asian J Trop Med Public Health 40 951 962

61. RatsitorahinaMHarisoaJRatovonjatoJBiacabeSReynesJM 2008 Outbreak of dengue and Chikungunya fevers, Toamasina, Madagascar, 2006. Emerg Infect Dis 14 1135 1137

62. TsetsarkinK 2009 Adaptation of chikungunya virus to aedes albopictus mosquitoes: the role of mutations in the e1 and e2 glycoproteins. Galveston The University of Texas Medical Branch 276

63. SmithDRAdamsAPKenneyJLWangEWeaverSC 2008 Venezuelan equine encephalitis virus in the mosquito vector Aedes taeniorhynchus: infection initiated by a small number of susceptible epithelial cells and a population bottleneck. Virology 372 176 186

64. TsetsarkinKHiggsSMcGeeCEDe LamballerieXCharrelRN 2006 Infectious clones of Chikungunya virus (La Reunion isolate) for vector competence studies. Vector Borne Zoonotic Dis 6 325 337

65. SambrookJFritschEManiatisT 1989 Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, , NY Cold Spring Harbor Laboratory

66. VanlandinghamDLTsetsarkinKHongCKlinglerKMcElroyKL 2005 Development and characterization of a double subgenomic chikungunya virus infectious clone to express heterologous genes in Aedes aegypti mosquitoes. Insect Biochem Mol Biol 35 1162 1170

67. GerbergEJ 1970 Manual for Mosquito Rearing and Experimental Techniques, Bulletin No. 5 Lake Charles, LA

68. VolkovaEGorchakovRFrolovI 2006 The efficient packaging of Venezuelan equine encephalitis virus-specific RNAs into viral particles is determined by nsP1-3 synthesis. Virology 344 315 327

69. HiggsSOlsonKEKamrudKIPowersAMBeatyBJ 1997 Viral expression systems and viral infections in insects. CramptonJMBeardCBLouisC The Molecular Biology of Disease Vectors: A Methods Manual UK Chapman & Hall 457 483

70. DeLanoWL 2006 PyMol molecular viewer. San Francisco, , CA DeLano Scientific LLC