Resistance of Echovirus 11 to ClO Is Associated with Enhanced Host Receptor Use, Altered Entry Routes, and High Fitness

Overview

Journal Environ Sci Technol

Publisher American Chemical Society

Specialty Environmental Health

Date 2017 Aug 25

PMID 28837336

Citations 12

Authors

Qingxia Zhong

Anna Carratala

Hyunjin Shim

Virginie Bachmann

Jeffrey D Jensen

Tamar Kohn

Affiliations

Soon will be listed here.

Abstract

Waterborne viruses can exhibit resistance to common water disinfectants, yet the mechanisms that allow them to tolerate disinfection are poorly understood. Here, we generated echovirus 11 (E11) with resistance to chlorine dioxide (ClO) by experimental evolution, and we assessed the associated genotypic and phenotypic traits. ClO resistance emerged after E11 populations were repeatedly reduced (either by ClO-exposure or by dilution) and then regrown in cell culture. The resistance was linked to an improved capacity of E11 to bind to its host cells, which was further attributed to two potential causes: first, the resistant E11 populations possessed mutations that caused amino acid substitutions from ClO-labile to ClO-stable residues in the viral proteins, which likely increased the chemical stability of the capsid toward ClO. Second, resistant E11 mutants exhibited the capacity to utilize alternative cell receptors for host binding. Interestingly, the emergence of ClO resistance resulted in an enhanced replicative fitness compared to the less resistant starting population. Overall this study contributes to a better understanding of the mechanism underlying disinfection resistance in waterborne viruses, and processes that drive resistance development.

Citing Articles

Genetic diversity of murine norovirus populations less susceptible to chlorine.

Wanguyun A, Oishi W, Rachmadi A, Katayama K, Sano D Front Microbiol. 2024; 15:1372641.

PMID: 38746753 PMC: 11091384. DOI: 10.3389/fmicb.2024.1372641.

Influence of Amino Acid Substitutions in Capsid Proteins of Coxsackievirus B5 on Free Chlorine and Thermal Inactivation.

Torii S, Gouttenoire J, Kumar K, Antanasijevic A, Kohn T Environ Sci Technol. 2024; 58(12):5279-5289.

PMID: 38488515 PMC: 10976892. DOI: 10.1021/acs.est.3c10409.

Echovirus 11 infection induces pyroptotic cell death by facilitating NLRP3 inflammasome activation.

Wang C, Yang R, Yang F, Han Y, Ren Y, Xiong X PLoS Pathog. 2022; 18(8):e1010787.

PMID: 36026486 PMC: 9455886. DOI: 10.1371/journal.ppat.1010787.

Chlorine Dioxide Inhibits African Swine Fever Virus by Blocking Viral Attachment and Destroying Viral Nucleic Acids and Proteins.

Wei R, Wang X, Cao Y, Gong L, Liu X, Zhang G Front Vet Sci. 2022; 9:844058.

PMID: 35372537 PMC: 8968399. DOI: 10.3389/fvets.2022.844058.

Effectiveness of two wastewater disinfection strategies for the removal of fecal indicator bacteria, bacteriophage, and enteric viral pathogens concentrated using dead-end hollow fiber ultrafiltration (D-HFUF).

Korajkic A, Kelleher J, Shanks O, Herrmann M, McMinn B Sci Total Environ. 2022; 831:154861.

PMID: 35358531 PMC: 9291237. DOI: 10.1016/j.scitotenv.2022.154861.

References

Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S . Rapid evolution of RNA genomes. Science. 1982; 215(4540):1577-85. DOI: 10.1126/science.7041255. View

Taylor M, Koyuncu O, Enquist L . Subversion of the actin cytoskeleton during viral infection. Nat Rev Microbiol. 2011; 9(6):427-39. PMC: 3229036. DOI: 10.1038/nrmicro2574. View

Okoh A, Sibanda T, Gusha S . Inadequately treated wastewater as a source of human enteric viruses in the environment. Int J Environ Res Public Health. 2010; 7(6):2620-37. PMC: 2905569. DOI: 10.3390/ijerph7062620. View

Zhong Q, Carratala A, Nazarov S, Guerrero-Ferreira R, Piccinini L, Bachmann V . Genetic, Structural, and Phenotypic Properties of MS2 Coliphage with Resistance to ClO Disinfection. Environ Sci Technol. 2016; 50(24):13520-13528. DOI: 10.1021/acs.est.6b04170. View

Strauss M, Filman D, Belnap D, Cheng N, Noel R, Hogle J . Nectin-like interactions between poliovirus and its receptor trigger conformational changes associated with cell entry. J Virol. 2015; 89(8):4143-57. PMC: 4442392. DOI: 10.1128/JVI.03101-14. View

Maillard J, Hann A, Perrin R . Resistance of Pseudomonas aeruginosa PAO1 phage F116 to sodium hypochlorite. J Appl Microbiol. 1998; 85(5):799-806. DOI: 10.1046/j.1365-2672.1998.00578.x. View

Smith J, Haigh J . The hitch-hiking effect of a favourable gene. Genet Res. 1974; 23(1):23-35. View

Stuart A, Eustace H, McKee T, Brown T . A novel cell entry pathway for a DAF-using human enterovirus is dependent on lipid rafts. J Virol. 2002; 76(18):9307-22. PMC: 136471. DOI: 10.1128/jvi.76.18.9307-9322.2002. View

Wigginton K, Pecson B, Sigstam T, Bosshard F, Kohn T . Virus inactivation mechanisms: impact of disinfectants on virus function and structural integrity. Environ Sci Technol. 2012; 46(21):12069-78. DOI: 10.1021/es3029473. View

10.

De Palma A, Vliegen I, De Clercq E, Neyts J . Selective inhibitors of picornavirus replication. Med Res Rev. 2008; 28(6):823-84. DOI: 10.1002/med.20125. View

11.

Winward G, Avery L, Stephenson T, Jefferson B . Chlorine disinfection of grey water for reuse: effect of organics and particles. Water Res. 2007; 42(1-2):483-91. DOI: 10.1016/j.watres.2007.07.042. View

12.

Triantafilou M, Wilson K, Triantafilou K . Identification of Echovirus 1 and coxsackievirus A9 receptor molecules via a novel flow cytometric quantification method. Cytometry. 2001; 43(4):279-89. DOI: 10.1002/1097-0320(20010401)43:4<279::aid-cyto1060>3.0.co;2-b. View

13.

Jin M, Zhao Z, Wang X, Shen Z, Xu L, Yu Y . The 40-80 nt region in the 5'-NCR of genome is a critical target for inactivating poliovirus by chlorine dioxide. J Med Virol. 2012; 84(3):526-35. DOI: 10.1002/jmv.23221. View

14.

Schmidtke M, Hammerschmidt E, Schuler S, Zell R, Birch-Hirschfeld E, Makarov V . Susceptibility of coxsackievirus B3 laboratory strains and clinical isolates to the capsid function inhibitor pleconaril: antiviral studies with virus chimeras demonstrate the crucial role of amino acid 1092 in treatment. J Antimicrob Chemother. 2005; 56(4):648-56. DOI: 10.1093/jac/dki263. View

15.

Xing L, Huhtala M, Pietiainen V, Kapyla J, Vuorinen K, Marjomaki V . Structural and functional analysis of integrin alpha2I domain interaction with echovirus 1. J Biol Chem. 2004; 279(12):11632-8. DOI: 10.1074/jbc.M312441200. View

16.

Chevaliez S, Balanant J, Maillard P, Lone Y, Lemonnier F, Delpeyroux F . Role of class I human leukocyte antigen molecules in early steps of echovirus infection of rhabdomyosarcoma cells. Virology. 2008; 381(2):203-14. DOI: 10.1016/j.virol.2008.08.006. View

17.

Thurston-Enriquez J, Haas C, Jacangelo J, Gerba C . Inactivation of enteric adenovirus and feline calicivirus by chlorine dioxide. Appl Environ Microbiol. 2005; 71(6):3100-5. PMC: 1151811. DOI: 10.1128/AEM.71.6.3100-3105.2005. View

18.

Kim C, Bergelson J . Echovirus 7 entry into polarized intestinal epithelial cells requires clathrin and Rab7. mBio. 2012; 3(2). PMC: 3324788. DOI: 10.1128/mBio.00304-11. View

19.

Krieger S, Kim C, Zhang L, Marjomaki V, Bergelson J . Echovirus 1 entry into polarized Caco-2 cells depends on dynamin, cholesterol, and cellular factors associated with macropinocytosis. J Virol. 2013; 87(16):8884-95. PMC: 3754084. DOI: 10.1128/JVI.03415-12. View

20.

He Y, Chipman P, Howitt J, Bator C, Whitt M, Baker T . Interaction of coxsackievirus B3 with the full length coxsackievirus-adenovirus receptor. Nat Struct Biol. 2001; 8(10):874-8. PMC: 4152846. DOI: 10.1038/nsb1001-874. View