Within-host whole-genome deep sequencing and diversity analysis of human respiratory syncytial virus infection reveals dynamics of genomic diversity in the absence and presence of immune pressure

Journal of Virology

Volumn 88, Issue 13, 2014, Pages 7286-7293

  Grad, Yonatan H ^a,b   Newman, Ruchi ^c   Zody, Michael ^c   Yang, Xiao ^c   Murphy, Ryan ^d   Qu, James ^c   Malboeuf, Christine M ^c   Levin, Joshua Z ^c   Lipsitch, Marc ^a   DeVincenzod, John ^d,e  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

^e LE BONHEUR CHILDREN'S MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; PALIVIZUMAB; VIRUS PROTEIN;

ADAPTIVE IMMUNITY; ARTICLE; BONE MARROW TRANSPLANTATION; CONTROLLED STUDY; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOTYPE; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOCOMPROMISED PATIENT; MICROBIAL DIVERSITY; MOLECULAR EPIDEMIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROSPECTIVE STUDY; RESPIRATORY SYNCYTIAL VIRUS INFECTION; SINGLE DRUG DOSE; T LYMPHOCYTE; VIRUS LOAD; VIRUS MUTATION; AMINO ACID SEQUENCE; GENETICS; GENOMICS; HIGH THROUGHPUT SEQUENCING; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOCOMPROMIZED PATIENT; IMMUNOLOGY; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; SEQUENCE HOMOLOGY; VIROLOGY; VIRUS GENOME;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; GENETIC VARIATION; GENOME, VIRAL; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IMMUNOCOMPROMISED HOST; MOLECULAR SEQUENCE DATA; PROSPECTIVE STUDIES; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL PROTEINS;

EID: 84901989752     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00038-14     Document Type: Article

References (37)

1. Hall CB. 2010. Respiratory syncytial virus, p 2207-2221. In Mandell GL, Bennett JE, Dolin R (ed), Principles and practice of infectious diseases, vol. 2. Churchill Livingstone Elsevier, Philadelphia, PA.
2. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE. 2005. Respiratory syncytial virus infection in elderly and high-risk adults. N. Engl. J. Med. 352:1749-1759. http://dx.doi.org/10.1056/NEJMoa043951.
3. Kim YJ, Boeckh M, Englund JA. 2007. Community respiratory virus infections in immunocompromised patients: hematopoietic stem cell and solid organ transplant recipients, and individuals with human immunodeficiency virus infection. Semin. Respir. Crit. Care Med. 28:222-242. http://dx.doi.org/10.1055/s-2007-976494.
4. Lujan-Zilbermann J, Benaim E, Tong X, Srivastava DK, Patrick CC, DeVincenzo JP. 2001. Respiratory virus infections in pediatric hematopoietic stem cell transplantation. Clin. Infect. Dis. 33:962-968. http://dx .doi.org/10.1086/322628.
5. Collins PL, Melero JA. 2011. Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res. 162: 80-99. http://dx.doi.org/10.1016/j.virusres.2011.09.020.
6. Glezen WP, Taber LH, Frank AL, Kasel JA. 1986. Risk of primary infection and reinfection with respiratory syncytial virus. Am. J. Dis. Child. 140:543-546.
7. Hall CB, Walsh EE, Schnabel KC, Long CE, McConnochie KM, Hildreth SW, Anderson LJ. 1990. Occurrence of groups A and B of respiratory syncytial virus over 15 years: associated epidemiologic and clinical characteristics in hospitalized and ambulatory children. J. Infect. Dis. 162: 1283-1290. http://dx.doi.org/10.1093/infdis/162.6.1283.
8. Peret TC, Hall CB, Hammond GW, Piedra PA, Storch GA, Sullender WM, Tsou C, Anderson LJ. 2000. Circulation patterns of group A and B human respiratory syncytial virus genotypes in 5 communities in North America. J. Infect. Dis. 181:1891-1896. http://dx.doi.org/10.1086/315508.
9. Peret TC, Hall CB, Schnabel KC, Golub JA, Anderson LJ. 1998. Circulation patterns of genetically distinct group A and B strains of human respiratory syncytial virus in a community. J. Gen. Virol. 79(Part 9):2221-2229.
10. Walsh EE, Falsey AR, Sullender WM. 1998. Monoclonal antibody neutralization escape mutants of respiratory syncytial virus with unique alterations in the attachment (G) protein. J. Gen. Virol. 79(Part 3):479-487.
11. Rueda P, Delgado T, Portela A, Melero JA, Garcia-Barreno B. 1991. Premature stop codons in the G glycoprotein of human respiratory syncytial viruses resistant to neutralization by monoclonal antibodies. J. Virol. 65:3374-3378.
12. Botosso VF, Zanotto PM, Ueda M, Arruda E, Gilio AE, Vieira SE, Stewien KE, Peret TC, Jamal LF, Pardini MI, Pinho JR, Massad E, Sant'anna OA, Holmes EC, Durigon EL. 2009. Positive selection results in frequent reversible amino acid replacements in the G protein gene of human respiratory syncytial virus. PLoS Pathog. 5:e1000254. http://dx.doi .org/10.1371/journal.ppat.1000254.
13. Tan L, Lemey P, Houspie L, Viveen MC, Jansen NJ, van Loon AM, Wiertz E, van Bleek GM, Martin DP, Coenjaerts FE. 2012. Genetic variability among complete human respiratory syncytial virus subgroup A genomes: bridging molecular evolutionary dynamics and epidemiology. PLoS One 7:e51439. http://dx.doi.org/10.1371/journal.pone.0051439.
14. Zlateva KT, Lemey P, Vandamme AM, Van Ranst M. 2004. Molecular evolution and circulation patterns of human respiratory syncytial virus subgroup A: positively selected sites in the attachment G glycoprotein. J. Virol. 78:4675-4683. http://dx.doi.org/10.1128/JVI.78.9.4675-4683.2004.
15. Oshansky CM, Zhang W, Moore E, Tripp RA. 2009. The host response and molecular pathogenesis associated with respiratory syncytial virus infection. Future Microbiol. 4:279-297. http://dx.doi.org/10.2217/fmb .09.1.
16. Henn MR, Boutwell C, Lennon N, Power K, Malboeuf C, Charlebois P, Gladden A, Levin J, Casali M, Philips L, Berlin A, Berical A, Erlich R, Anderson S, Streeck H, Kemper M, Ryan E, Wang Y, Green L, Axten K, Brumme Z, Brumme C, Russ C, Rosenberg E, Jessen H, Altfeld M, Nusbaum C, Walker B, Birren B, Allen TM. 2009. P09-20 LB. Ultradeep sequencing of full-length HIV-1 genomes identifies rapid viral evolution during acute infection. Retrovirology 6:P400. http://dx.doi.org/10 .1186/1742-4690-6-S3-P400.
17. Tsibris AM, Korber B, Arnaout R, Russ C, Lo CC, Leitner T, Gaschen B, Theiler J, Paredes R, Su Z, Hughes MD, Gulick RM, Greaves W, Coakley E, Flexner C, Nusbaum C, Kuritzkes DR. 2009. Quantitative deep sequencing reveals dynamic HIV-1 escape and large population shifts during CCR5 antagonist therapy in vivo. PLoS One 4:e5683. http: //dx.doi.org/10.1371/journal.pone.0005683.
18. Grenfell BT, Pybus OG, Gog JR, Wood JL, Daly JM, Mumford JA, Holmes EC. 2004. Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303:327-332. http://dx.doi.org/10.1126/science .1090727.
19. El Saleeby CM, Suzich J, Conley ME, DeVincenzo JP. 2004. Quantitative effects of palivizumab and donor-derived T cells on chronic respiratory syncytial virus infection, lung disease, and fusion glycoprotein amino acid sequences in a patient before and after bone marrow transplantation. Clin. Infect. Dis. 39:e17-20. http://dx.doi.org/10.1086/421779.
20. Malboeuf CM, Yang X, Charlebois P, Qu J, Berlin AM, Casali M, Pesko KN, Boutwell CL, DeVincenzo JP, Ebel GD, Allen TM, Zody MC, Henn MR, Levin JZ. 2013. Complete viral RNA genome sequencing of ultra-low copy samples by sequence-independent amplification. Nucleic Acids Res. 41:e13. http://dx.doi.org/10.1093/nar/gks794.
21. Yang X, Charlebois P, Gnerre S, Coole MG, Lennon NJ, Levin JZ, Qu J, Ryan EM, Zody MC, Henn MR. 2012. De novo assembly of highly diverse viral populations. BMC Genomics 13:475. http://dx.doi.org/10 .1186/1471-2164-13-475.
22. Yang X, Charlebois P, Macalalad A, Henn MR, Zody MC. 2013. VPhaser 2: variant inference for viral populations. BMC Genomics 14:674. http://dx.doi.org/10.1186/1471-2164-14-674.
23. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188-1190. http://dx.doi.org /10.1101/gr.849004.
24. Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27:221-224. http://dx.doi.org/10.1093 /molbev/msp259.
25. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, Wei X, Jiang C, Kirchherr JL, Gao F, Anderson JA, Ping LH, Swanstrom R, Tomaras GD, Blattner WA, Goepfert PA, Kilby JM, Saag MS, Delwart EL, Busch MP, Cohen MS, Montefiori DC, Haynes BF, Gaschen B, Athreya GS, Lee HY, Wood N, Seoighe C, Perelson AS, Bhattacharya T, Korber BT, Hahn BH, Shaw GM. 2008. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 105:7552-7557. http://dx.doi.org/10.1073/pnas.0802203105.
26. Bukreyev A, Yang L, Fricke J, Cheng L, Ward JM, Murphy BR, Collins PL. 2008. The secreted form of respiratory syncytial virus G glycoprotein helps the virus evade antibody-mediated restriction of replication by act-ing as an antigen decoy and through effects on Fc receptor-bearing leukocytes. J. Virol. 82:12191-12204. http://dx.doi.org/10.1128/JVI.01604-08.
27. Melero JA, Garcia-Barreno B, Martinez I, Pringle CR, Cane PA. 1997. Antigenic structure, evolution and immunobiology of human respiratory syncytial virus attachment (G) protein. J. Gen. Virol. 78(Part 10):2411-2418.
28. Shingai M, Azuma M, Ebihara T, Sasai M, Funami K, Ayata M, Ogura H, Tsutsumi H, Matsumoto M, Seya T. 2008. Soluble G protein of respiratory syncytial virus inhibits Toll-like receptor 3/4-mediated IFNbeta induction. Int. Immunol. 20:1169-1180. http://dx.doi.org/10.1093 /intimm/dxn074.
29. Venter M, van Niekerk S, Rakgantso A, Bent N. 2011. Identification of deletion mutant respiratory syncytial virus strains lacking most of the G protein in immunocompromised children with pneumonia in South Africa. J. Virol. 85:8453-8457. http://dx.doi.org/10.1128/JVI.00674-11.
30. Techaarpornkul S, Barretto N, Peeples ME. 2001. Functional analysis of recombinant respiratory syncytial virus deletion mutants lacking the small hydrophobic and/or attachment glycoprotein gene. J. Virol. 75:6825-6834. http://dx.doi.org/10.1128/JVI.75.15.6825-6834.2001.
31. Teng MN, Whitehead SS, Collins PL. 2001. Contribution of the respiratory syncytial virus G glycoprotein and its secreted and membranebound forms to virus replication in vitro and in vivo. Virology 289:283-296. http://dx.doi.org/10.1006/viro.2001.1138.
32. Zhao X, Chen FP, Megaw AG, Sullender WM. 2004. Variable resistance to palivizumab in cotton rats by respiratory syncytial virus mutants. J. Infect. Dis. 190:1941-1946. http://dx.doi.org/10.1086/425515.
33. Zhu Q, McAuliffe JM, Patel NK, Palmer-Hill FJ, Yang CF, Liang B, Su L, Zhu W, Wachter L, Wilson S, MacGill RS, Krishnan S, McCarthy MP, Losonsky GA, Suzich JA. 2011. Analysis of respiratory syncytial virus preclinical and clinical variants resistant to neutralization by monoclonal antibodies palivizumab and/or motavizumab. J. Infect. Dis. 203:674-682. http://dx.doi.org/10.1093/infdis/jiq100.
34. Zhu Q, Patel NK, McAuliffe JM, Zhu W, Wachter L, McCarthy MP, Suzich JA. 2012. Natural polymorphisms and resistance-associated mutations in the fusion protein of respiratory syncytial virus (RSV): effects on RSV susceptibility to palivizumab. J. Infect. Dis. 205:635-638. http://dx .doi.org/10.1093/infdis/jir790.
35. Papenburg J, Carbonneau J, Hamelin ME, Isabel S, Bouhy X, Ohoumanne N, Dery P, Paes BA, Corbeil J, Bergeron MG, De Serres G, Boivin G. 2012. Molecular evolution of respiratory syncytial virus fusion gene, Canada, 2006-2010. Emerg. Infect. Dis. 18:120-124. http://dx.doi .org/10.3201/eid1801.110515.
36. Wu H, Pfarr DS, Johnson S, Brewah YA, Woods RM, Patel NK, White WI, Young JF, Kiener PA. 2007. Development of motavizumab, an ultra-potent antibody for the prevention of respiratory syncytial virus infection in the upper and lower respiratory tract. J. Mol. Biol. 368:652-665. http://dx.doi.org/10.1016/j.jmb.2007.02.024.
37. Kryazhimskiy S, Plotkin JB. 2008. The population genetics of dN/dS. PLoS Genet. 4:e1000304. http://dx.doi.org/10.1371/journal.pgen.1000304.