Quantitative insertion-site sequencing (QIseq) for high throughput phenotyping of transposon mutants

Genome Research

Volumn 26, Issue 7, 2016, Pages 980-989

  Bronner, Iraad F ^a   Otto, Thomas D ^a   Zhang, Min ^b   Udenze, Kenneth ^b   Wang, Chengqi ^b   Quail, Michael A ^a   Jiang, Rays H Y ^b   Adams, John H ^b   Rayner, Julian C ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMISININ; PROTEIN; TRANSPOSON;

ANTIMALARIAL DRUG RESISTANCE; ARTICLE; GENE INSERTION; GENETIC ANALYZER; GENETIC SCREENING; GENETIC TRANSFECTION; GENOME ANALYSIS; HIGH THROUGHPUT SEQUENCING; INVERTED TERMINAL REPEAT; MOLECULAR LIBRARY; MONITORING; MUTANT; MUTATION; NONHUMAN; PHENOTYPE; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; QUANTITATIVE INSERTION SITE SEQUENCING; REPRODUCIBILITY; SCALE UP; SENSITIVITY AND SPECIFICITY; TRANSPOSON; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENE LIBRARY; GENE ONTOLOGY; GENETICS; NUCLEOTIDE SEQUENCE;

BASE SEQUENCE; DNA TRANSPOSABLE ELEMENTS; GENE LIBRARY; GENE ONTOLOGY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MUTAGENESIS, INSERTIONAL; PHENOTYPE; PLASMODIUM FALCIPARUM; SEQUENCE ANALYSIS, DNA;

EID: 84976889195     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.200279.115     Document Type: Article

References (37)

1. Alsford S, Turner DJ, Obado SO, Sanchez-Flores A, Glover L, Berriman M, Hertz-Fowler C, Horn D. 2011. High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res 21: 915-924.
2. Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois AC, Khim N, Kim S, Duru V, Bouchier C, Ma L, et al. 2014. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505: 50-55.
3. Ashley EA, Dhorda M, Fairhurst RM, Amaratunga C, Lim P, Suon S, Sreng S, Anderson JM, Mao S, Sam B, et al. 2014. Spread of artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 371: 411-423.
4. Balu B, Shoue DA, Fraser MJ Jr., Adams JH. 2005. High-efficiency transformation of Plasmodium falciparum by the lepidopteran transposable element piggyBac. Proc Natl Acad Sci 102: 16391-16396.
5. Balu B, Chauhan C, Maher SP, Shoue DA, Kissinger JC, Fraser MJ Jr., Adams JH. 2009. piggyBac is an effective tool for functional analysis of the Plasmodium falciparum genome. BMC Microbiol 9: 83.
6. Balu B, Singh N, Maher SP, Adams JH. 2010. A genetic screen for attenuated growth identifies genes crucial for intraerythrocytic development of Plasmodium falciparum. PLoS One 5: e13282.
7. Cary LC, Goebel M, Corsaro BG, Wang HG, Rosen E, Fraser MJ. 1989. Transposon mutagenesis of baculoviruses: analysis of Trichoplusia ni transposon IFP2 insertions within the FP-locus of nuclear polyhedrosis viruses. Virology 172: 156-169.
8. Cowman AF, Berry D, Baum J. 2012. The cellular and molecular basis for malaria parasite invasion of the human red blood cell. J Cell Biol 198: 961-971.
9. Ekland EH, Fidock DA. 2007. Advances in understanding the genetic basis of antimalarial drug resistance. Curr Opin Microbiol 10: 363-370.
10. Fonager J, Franke-Fayard BM, Adams JH, Ramesar J, Klop O, Khan SM, Janse CJ, Waters AP. 2011. Development of the piggyBac transposable system for Plasmodium berghei and its application for random mutagenesis in malaria parasites. BMC Genomics 12: 155.
11. Fraser MJ, Cary L, Boonvisudhi K, Wang HG. 1995. Assay for movement of Lepidopteran transposon IFP2 in insect cells using a baculovirus genome as a target DNA. Virology 211: 397-407.
12. Friedel RH, Friedel CC, Bonfert T, Shi R, Rad R, Soriano P. 2013. Clonal expansion analysis of transposon insertions by high-throughput sequencing identifies candidate cancer genes in a PiggyBac mutagenesis screen. PLoS One 8: e72338.
13. Gallagher LA, Shendure J, Manoil C. 2011. Genome-scale identification of resistance functions in Pseudomonas aeruginosa using Tn-seq. MBio 2: e00315-10.
14. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
15. Gawronski JD, Wong SM, Giannoukos G, Ward DV, Akerley BJ. 2009. Tracking insertion mutants within libraries by deep sequencing and a genome-wide screen for Haemophilus genes required in the lung. Proc Natl Acad Sci 106: 16422-16427.
16. Ghorbal M, Gorman M, Macpherson CR, Martins RM, Scherf A, Lopez-Rubio JJ. 2014. Genome editing in the human malaria parasite Plasmodium falciparum using the CRISPR-Cas9 system. Nat Biotechnol 32: 819-821.
17. Gomes AR, Bushell E, Schwach F, Girling G, Anar B, Quail MA, Herd C, Pfander C, Modrzynska K, Rayner JC, et al. 2015. A genome-scale vector resource enables high-throughput reverse genetic screening in a malaria parasite. Cell Host Microbe 17: 404-413.
18. Gonzalez-Estevez C, Momose T, Gehring WJ, Salo E. 2003. Transgenic planarian lines obtained by electroporation using transposon-derived vectors and an eye-specific GFP marker. Proc Natl Acad Sci 100: 14046-14051.
19. Goodman AL, McNulty NP, Zhao Y, Leip D, Mitra RD, Lozupone CA, Knight R, Gordon JI. 2009. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 6: 279-289.
20. Goranov AI, Madhani HD. 2014. Functional profiling of human fungal pathogen genomes. Cold Spring Harb Perspect Med 5: a019596.
21. Hayward R, Saliba KJ, Kirk K. 2005. pfmdr1 mutations associated with chloroquine resistance incur a fitness cost in Plasmodium falciparum. Mol Microbiol 55: 1285-1295.
22. Ikadai H, Shaw Saliba K, Kanzok SM, McLean KJ, Tanaka TQ, Cao J, Williamson KC, Jacobs-Lorena M. 2013. Transposon mutagenesis identifies genes essential for Plasmodium falciparum gametocytogenesis. Proc Natl Acad Sci 110: E1676-E1684.
23. Langridge GC, Phan MD, Turner DJ, Perkins TT, Parts L, Haase J, Charles I, Maskell DJ, Peters SE, Dougan G, et al. 2009. Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Res 19: 2308-2316.
24. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
25. malERA Consultative Group on Vaccines. 2011. A research agenda for malaria eradication: vaccines. PLoS Med 8: e1000398.
26. Moll K, Ljungström I, Perlmann H, Scherf A, Wahlgren M. 2008. Methods in malaria research, 5th ed. MR4/ATCC, Manassas, VA.
27. Pradhan A, Siwo GH, Singh N, Martens B, Balu B, Button-Simons KA, Tan A, Zhang M, Udenze KO, Jiang RH, et al. 2015. Chemogenomic profiling of Plasmodium falciparum as a tool to aid antimalarial drug discovery. Sci Rep 5: 15930.
28. R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
29. Rad R, Rad L, WangW, Cadinanos J, Vassiliou G, Rice S, Campos LS, Yusa K, Banerjee R, Li MA, et al. 2010. PiggyBac transposon mutagenesis: a tool for cancer gene discovery in mice. Science 330: 1104-1107.
30. Rad R, Rad L, Wang W, Strong A, Ponstingl H, Bronner IF, Mayho M, Steiger K, Weber J, Hieber M, et al. 2015. A conditional piggyBac transposition system for genetic screening in mice identifies oncogenic networks in pancreatic cancer. Nat Genet 47: 47-56.
31. Rinaldi G, Eckert SE, Tsai IJ, Suttiprapa S, Kines KJ, Tort JF, Mann VH, Turner DJ, Berriman M, Brindley PJ. 2012. Germline transgenesis and insertional mutagenesis in Schistosoma mansoni mediated by murine leukemia virus. PLoS Pathog 8: e1002820.
32. Simpson JT, Durbin R. 2012. Efficient de novo assembly of large genomes using compressed data structures. Genome Res 22: 549-556.
33. Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA, Singh CM, Buchholz R, Demsky M, Fawcett R, Francis-Lang HL, et al. 2004. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 36: 283-287.
34. Uren AG, Mikkers H, Kool J, van der Weyden L, Lund AH, Wilson CH, Rance R, Jonkers J, van Lohuizen M, Berns A, et al. 2009. A high-throughput splinkerette-PCR method for the isolation and sequencing of retroviral insertion sites. Nat Protoc 4: 789-798.
35. van Opijnen T, Bodi KL, Camilli A. 2009. Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms. Nat Methods 6: 767-772.
36. Wagner JC, Platt RJ, Goldfless SJ, Zhang F, Niles JC. 2014. Efficient CRISPRCas9-mediated genome editing in Plasmodium falciparum. Nat Methods 11: 915-918.
37. WuSC, Meir YJ, Coates CJ, Handler AM, Pelczar P, Moisyadi S, Kaminski JM. 2006. piggyBac is a flexible and highly active transposon as compared to Sleeping Beauty, Tol2, and Mos1 in mammalian cells. Proc Natl Acad Sci 103: 15008-15013.