Complete viral RNA genome sequencing of ultra-low copy samples by sequence-independent amplification

Nucleic Acids Research

Volumn 41, Issue 1, 2013, Pages

  Malboeuf, Christine M ^a   Yang, Xiao ^a   Charlebois, Patrick ^a   Qu, James ^a   Berlin, Aaron M ^a   Casali, Monica ^a   Pesko, Kendra N ^b,f   Boutwell, Christian L ^c   Devincenzo, John P ^d,e   Ebel, Gregory D ^b,g   Allen, Todd M ^c   Zody, Michael C ^a   Henn, Matthew R ^a   Levin, Joshua Z ^a  

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

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

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

^e UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^f YALE UNIVERSITY   (United States)

^g Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS PROTEIN; VIRUS RNA;

ARTICLE; GENE AMPLIFICATION; GENE DOSAGE; GENE TARGETING; GENETIC CODE; HUMAN IMMUNODEFICIENCY VIRUS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; RNA SEQUENCE; SAMPLE SIZE; VIRUS ASSEMBLY; VIRUS GENOME; VIRUS LOAD; WEST NILE FLAVIVIRUS;

BASE SEQUENCE; GENOME, VIRAL; HIV; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID AMPLIFICATION TECHNIQUES; RESPIRATORY SYNCYTIAL VIRUSES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, VIRAL; SEQUENCE ANALYSIS, RNA; WEST NILE VIRUS;

RNA VIRUSES;

EID: 84867398590     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks794     Document Type: Article

References (49)

1. Bimber, B.N., Dudley, D.M., Lauck, M., Becker, E.A., Chin, E.N., Lank, S.M., Grunenwald, H.L., Caruccio, N.C., Maffitt, M., Wilson, N.A. et al. (2010) Whole-genome characterization of human and simian immunodeficiency virus intrahost diversity by ultradeep pyrosequencing. J. Virol., 84, 12087-12092.
2. Fischer, W., Ganusov, V.V., Giorgi, E.E., Hraber, P.T., Keele, B.F., Leitner, T., Han, C.S., Gleasner, C.D., Green, L., Lo, C.C. et al. (2010) Transmission of single HIV-1 genomes and dynamics of early immune escape revealed by ultra-deep sequencing. PLoS One, 5, e12303.
3. Hoffmann, C., Minkah, N., Leipzig, J., Wang, G., Arens, M.Q., Tebas, P. and Bushman, F.D. (2007) DNA bar coding and pyrosequencing to identify rare HIV drug resistance mutations. Nucleic Acids Res., 35, e91.
4. Simen, B.B., Simons, J.F., Hullsiek, K.H., Novak, R.M., Macarthur, R.D., Baxter, J.D., Huang, C., Lubeski, C., Turenchalk, G.S., Braverman, M.S. et al. (2009) Low-abundance drug-resistant viral variants in chronically HIV-infected, antiretroviral treatment-naive patients significantly impact treatment outcomes. J. Infect. Dis., 199, 693-701.
5. Tsibris, A.M., Korber, B., Arnaout, R., Russ, C., Lo, C.C., Leitner, T., Gaschen, B., Theiler, J., Paredes, R., Su, Z. et al. (2009) Quantitative deep sequencing reveals dynamic HIV-1 escape and large population shifts during CCR5 antagonist therapy in vivo. PLoS One, 4, e5683.
6. Wang, C., Mitsuya, Y., Gharizadeh, B., Ronaghi, M. and Shafer, R.W. (2007) Characterization of mutation spectra with ultra-deep pyrosequencing: application to HIV-1 drug resistance. Genome Res., 17, 1195-1201.
7. Wang, G.P., Sherrill-Mix, S.A., Chang, K.M., Quince, C. and Bushman, F.D. (2010) Hepatitis C virus transmission bottlenecks analyzed by deep sequencing. J. Virol., 84, 6218-6228.
8. Lauck, M., Alvarado-Mora, M.V., Becker, E.A., Bhattacharya, D., Striker, R., Hughes, A.L., Carrilho, F.J., O'Connor, D.H. and Pinho, J.R. (2012) Analysis of hepatitis C virus intrahost diversity across the coding region by ultradeep pyrosequencing. J. Virol., 86, 3952-3960.
9. Pesko, K.N., Fitzpatrick, K.A., Ryan, E.M., Shi, P.Y., Zhang, B., Lennon, N.J., Newman, R.M., Henn, M.R. and Ebel, G.D. (2012) Internally deleted WNV genomes isolated from exotic birds in New Mexico: function in cells, mosquitoes, and mice. Virology, 427, 10-17.
10. Henn, M.R., Boutwell, C.L., Charlebois, P., Lennon, N.J., Power, K.A., Macalalad, A.R., Berlin, A.M., Malboeuf, C.M., Ryan, E.M., Gnerre, S. et al. (2012) Whole genome deep sequencing of HIV-1 reveals the impact of early minor variants upon immune recognition during acute infection. PLoS Pathog., 8, e1002529.
11. Parameswaran, P., Charlebois, P., Tellez, Y., Nunez, A., Ryan, E.M., Malboeuf, C.M., Levin, J.Z., Lennon, N.J., Balmaseda, A., Harris, E. et al. (2012) Genome-wide patterns of intra-human dengue virus diversity reveal associations with viral phylogenetic clade and inter-host diversity. J Virol., 86, 8546-8558.
12. Cordey, S., Junier, T., Gerlach, D., Gobbini, F., Farinelli, L., Zdobnov, E.M., Winther, B., Tapparel, C. and Kaiser, L. (2010) Rhinovirus genome evolution during experimental human infection. PLoS One, 5, e10588.
13. Eckerle, L.D., Becker, M.M., Halpin, R.A., Li, K., Venter, E., Lu, X., Scherbakova, S., Graham, R.L., Baric, R.S., Stockwell, T.B. et al. (2010) Infidelity of SARS-CoV Nsp14-exonuclease mutant virus replication is revealed by complete genome sequencing. PLoS Pathog., 6, e1000896.
14. Wright, C.F., Morelli, M.J., Thebaud, G., Knowles, N.J., Herzyk, P., Paton, D.J., Haydon, D.T. and King, D.P. (2010) Beyond the consensus: dissecting within-host viral population diversity of foot-and-mouth disease virus using next-generation genome sequencing. J. Virol., 85, 2266-2275.
15. Miura, T., Brockman, M.A., Brumme, C.J., Brumme, Z.L., Carlson, J.M., Pereyra, F., Trocha, A., Addo, M.M., Block, B.L., Rothchild, A.C. et al. (2008) Genetic characterization of human immunodeficiency virus type 1 in elite controllers: lack of gross genetic defects or common amino acid changes. J. Virol., 82, 8422-8430.
16. Palmer, S., Kearney, M., Maldarelli, F., Halvas, E.K., Bixby, C.J., Bazmi, H., Rock, D., Falloon, J., Davey, R.T. Jr, Dewar, R.L. et al. (2005) Multiple, linked human immunodeficiency virus type 1 drug resistance mutations in treatment-experienced patients are missed by standard genotype analysis. J. Clin. Microbiol., 43, 406-413.
17. Salazar-Gonzalez, J.F., Bailes, E., Pham, K.T., Salazar, M.G., Guffey, M.B., Keele, B.F., Derdeyn, C.A., Farmer, P., Hunter, E., Allen, S. et al. (2008) Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J. Virol., 82, 3952-3970.
18. Deeks, S.G. and Walker, B.D. (2007) Human immunodeficiency virus controllers: mechanisms of durable virus control in the absence of antiretroviral therapy. Immunity, 27, 406-416.
19. Tricou, V., Minh, N.N., Farrar, J., Tran, H.T. and Simmons, C.P. (2011) Kinetics of viremia and NS1 antigenemia are shaped by immune status and virus serotype in adults with dengue. PLoS Negl. Trop. Dis., 5, e1309.
20. Gu, W., Unnasch, T.R., Katholi, C.R., Lampman, R. and Novak, R.J. (2008) Fundamental issues in mosquito surveillance for arboviral transmission. Trans. R. Soc. Trop. Med. Hyg., 102, 817-822.
21. Cheval, J., Sauvage, V., Frangeul, L., Dacheux, L., Guigon, G., Dumey, N., Pariente, K., Rousseaux, C., Dorange, F., Berthet, N. et al. (2011) Evaluation of high-throughput sequencing for identifying known and unknown viruses in biological samples. J. Clin. Microbiol., 49, 3268-3275.
22. Djikeng, A., Halpin, R., Kuzmickas, R., Depasse, J., Feldblyum, J., Sengamalay, N., Afonso, C., Zhang, X., Anderson, N.G., Ghedin, E. et al. (2008) Viral genome sequencing by random priming methods. BMC Genomics, 9, 5.
23. Ninomiya, M., Ueno, Y., Funayama, R., Nagashima, T., Nishida, Y., Kondo, Y., Inoue, J., Kakazu, E., Kimura, O., Nakayama, K. et al. (2012) Use of illumina deep sequencing technology to differentiate hepatitis C virus variants. J. Clin. Microbiol., 50, 857-866.
24. Moore, R.A., Warren, R.L., Freeman, J.D., Gustavsen, J.A., Chenard, C., Friedman, J.M., Suttle, C.A., Zhao, Y. and Holt, R.A. (2011) The sensitivity of massively parallel sequencing for detecting candidate infectious agents associated with human tissue. PLoS One, 6, e19838.
25. Victoria, J.G., Kapoor, A., Li, L., Blinkova, O., Slikas, B., Wang, C., Naeem, A., Zaidi, S. and Delwart, E. (2009) Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J. Virol., 83, 4642-4651.
26. Beane, J., Vick, J., Schembri, F., Anderlind, C., Gower, A., Campbell, J., Luo, L., Zhang, X.H., Xiao, J., Alekseyev, Y.O. et al. (2011) Characterizing the impact of smoking and lung cancer on the airway transcriptome using RNA-Seq. Cancer Prev. Res. (Phila), 4, 803-817.
27. Tariq, M.A., Kim, H.J., Jejelowo, O. and Pourmand, N. (2011) Whole-transcriptome RNAseq analysis from minute amount of total RNA. Nucleic Acids Res., 39, e120.
28. Adachi, A., Gendelman, H.E., Koenig, S., Folks, T., Willey, R., Rabson, A. and Martin, M.A. (1986) Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol., 59, 284-291.
29. Shi, P.Y., Tilgner, M., Lo, M.K., Kent, K.A. and Bernard, K.A. (2002) Infectious cDNA clone of the epidemic west nile virus from New York City. J. Virol., 76, 5847-5856.
30. Devincenzo, J.P. (2004) Natural infection of infants with respiratory syncytial virus subgroups A and B: a study of frequency, disease severity, and viral load. Pediatr. Res., 56, 914-917.
31. Christopherson, C., Sninsky, J. and Kwok, S. (1997) The effects of internal primer-template mismatches on RT-PCR: HIV-1 model studies. Nucleic Acids Res., 25, 654-658.
32. Kauffman, E.B., Jones, S.A., Dupuis, A.P. 2nd, Ngo, K.A., Bernard, K.A. and Kramer, L.D. (2003) Virus detection protocols for west nile virus in vertebrate and mosquito specimens. J. Clin. Microbiol., 41, 3661-3667.
33. Perkins, S.M., Webb, D.L., Torrance, S.A., El Saleeby, C., Harrison, L.M., Aitken, J.A., Patel, A. and DeVincenzo, J.P. (2005) Comparison of a real-time reverse transcriptase PCR assay and a culture technique for quantitative assessment of viral load in children naturally infected with respiratory syncytial virus. J. Clin. Microbiol., 43, 2356-2362.
34. Kurn, N., Chen, P., Heath, J.D., Kopf-Sill, A., Stephens, K.M. and Wang, S. (2005) Novel isothermal, linear nucleic acid amplification systems for highly multiplexed applications. Clin. Chem., 51, 1973-1981.
35. Levin, J.Z., Yassour, M., Adiconis, X., Nusbaum, C., Thompson, D.A., Friedman, N., Gnirke, A. and Regev, A. (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat. Methods, 7, 709-715.
36. Huson, D.H., Mitra, S., Ruscheweyh, H.J., Weber, N. and Schuster, S.C. (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res., 21, 1552-1560.
37. Zhang, Z., Schwartz, S., Wagner, L. and Miller, W. (2000) A greedy algorithm for aligning DNA sequences. J. Comput. Biol., 7, 203-214.
38. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797.
39. Willerth, S.M., Pedro, H.A., Pachter, L., Humeau, L.M., Arkin, A.P. and Schaffer, D.V. (2010) Development of a low bias method for characterizing viral populations using next generation sequencing technology. PLoS One, 5, e13564.
40. Li, R., Zhu, H., Ruan, J., Qian, W., Fang, X., Shi, Z., Li, Y., Li, S., Shan, G., Kristiansen, K. et al. (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res., 20, 265-272.
41. Archer, J., Rambaut, A., Taillon, B.E., Harrigan, P.R., Lewis, M. and Robertson, D.L. (2010) The evolutionary analysis of emerging low frequency HIV-1 CXCR4 using variants through time-an ultra-deep approach. PLoS Comput. Biol., 6, e1001022.
42. Watts, J.M., Dang, K.K., Gorelick, R.J., Leonard, C.W., Bess, J.W. Jr, Swanstrom, R., Burch, C.L. and Weeks, K.M. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature, 460, 711-716.
43. Hofacker, I.L., Stadler, P.F. and Stocsits, R.R. (2004) Conserved RNA secondary structures in viral genomes: a survey. Bioinformatics, 20, 1495-1499.
44. Harrison, G.P., Mayo, M.S., Hunter, E. and Lever, A.M. (1998) Pausing of reverse transcriptase on retroviral RNA templates is influenced by secondary structures both 5' and 3' of the catalytic site. Nucleic Acids Res., 26, 3433-3442.
45. Adey, A., Morrison, H.G., Asan., Xun, X., Kitzman, J.O., Turner, E.H., Stackhouse, B., MacKenzie, A.P., Caruccio, N.C., Zhang, X. et al. (2010) Rapid, low-input, low-bias construction of shotgun fragment libraries by high-density in vitro transposition. Genome Biol., 11, R119.
46. Marine, R., Polson, S.W., Ravel, J., Hatfull, G., Russell, D., Sullivan, M., Syed, F., Dumas, M. and Wommack, K.E. (2011) Evaluation of a transposase protocol for rapid generation of shotgun high-throughput sequencing libraries from nanogram quantities of DNA. Appl. Environ. Microbiol., 77, 8071-8079.
47. ten Bosch, J.R., Deignan, J.L. and Grody, W.W. (2011) Next-generation Sequencing in Clinical Molecular Diagnostics. John Wiley, New York.
48. Dong, J., Olano, J.P., McBride, J.W. and Walker, D.H. (2008) Emerging pathogens: challenges and successes of molecular diagnostics. J. Mol. Diagn., 10, 185-197.
49. Morin, R., Bainbridge, M., Fejes, A., Hirst, M., Krzywinski, M., Pugh, T., McDonald, H., Varhol, R., Jones, S. and Marra, M. (2008) Profiling the HeLa S3 transcriptome using randomly primed cDNA and massively parallel short-read sequencing. Biotechniques, 45, 81-94.