Transcriptome Profiling of Giardia intestinalis Using Strand-specific RNA-Seq

PLoS Computational Biology

Volumn 9, Issue 3, 2013, Pages

  Franzén, Oscar ^a   Jerlström Hultqvist, Jon ^b   Einarsson, Elin ^b   Ankarklev, Johan ^b   Ferella, Marcela ^b   Andersson, Björn ^a   Svärd, Staffan G ^b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

PROTOZOA; TRANSCRIPTION;

'CURRENT; GENES EXPRESSION; GENOME ANNOTATION; GENOME SEQUENCES; GIARDIA; GIARDIA INTESTINALIS; HOST-SPECIFICITY; IN-VITRO; TRANSCRIPTOME PROFILING; TRANSCRIPTOMES;

RNA;

TRANSCRIPTOME;

3' UNTRANSLATED REGION; ALLELE; ARTICLE; CHROMOSOME 5; CONTROLLED STUDY; GENE CLUSTER; GENE DOSAGE; GENE MAPPING; GENETIC CONSERVATION; GENETIC VARIABILITY; GIARDIA LAMBLIA; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PARASITE ISOLATION; PHYLOGENY; POLYADENYLATION; RNA ANALYSIS; RNA SEQUENCE; RNA SPLICING;

EID: 84875999387     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003000     Document Type: Article

References (71)

1. Ankarklev J, Jerlstrom-Hultqvist J, Ringqvist E, Troell K, Svard SG, (2010) Behind the smile: cell biology and disease mechanisms of Giardia species. Nat Rev Microbiol 8: 413-422.
2. Monis PT, Caccio SM, Thompson RC, (2009) Variation in Giardia: towards a taxonomic revision of the genus. Trends Parasitol 25: 93-100.
3. Thompson RC, (2004) The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Vet Parasitol 126: 15-35.
4. Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, et al. (2007) Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317: 1921-1926.
5. Franzen O, Jerlstrom-Hultqvist J, Castro E, Sherwood E, Ankarklev J, et al. (2009) Draft genome sequencing of giardia intestinalis assemblage B isolate GS: is human giardiasis caused by two different species? PLoS Pathog 5: e1000560.
6. Jerlstrom-Hultqvist J, Franzen O, Ankarklev J, Xu F, Nohynkova E, et al. (2010) Genome analysis and comparative genomics of a Giardia intestinalis assemblage E isolate. BMC Genomics 11: 543.
7. Elmendorf HG, Singer SM, Pierce J, Cowan J, Nash TE, (2001) Initiator and upstream elements in the alpha2-tubulin promoter of Giardia lamblia. Mol Biochem Parasitol 113: 157-169.
8. Knodler LA, Svard SG, Silberman JD, Davids BJ, Gillin FD, (1999) Developmental gene regulation in Giardia lamblia: first evidence for an encystation-specific promoter and differential 5′ mRNA processing. Mol Microbiol 34: 327-340.
9. Sun CH, Palm D, McArthur AG, Svard SG, Gillin FD, (2002) A novel Myb-related protein involved in transcriptional activation of encystation genes in Giardia lamblia. Mol Microbiol 46: 971-984.
10. Davis-Hayman SR, Hayman JR, Nash TE, (2003) Encystation-specific regulation of the cyst wall protein 2 gene in Giardia lamblia by multiple cis-acting elements. Int J Parasitol 33: 1005-1012.
11. Baldauf SL, (2003) The deep roots of eukaryotes. Science 300: 1703-1706.
12. Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF, (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290: 972-977.
13. Best AA, Morrison HG, McArthur AG, Sogin ML, Olsen GJ, (2004) Evolution of eukaryotic transcription: insights from the genome of Giardia lamblia. Genome Res 14: 1537-1547.
14. Williams CW, Elmendorf HG, (2011) Identification and analysis of the RNA degrading complexes and machinery of Giardia lamblia using an in silico approach. BMC Genomics 12: 586.
15. Chen YH, Su LH, Huang YC, Wang YT, Kao YY, et al. (2008) UPF1, a conserved nonsense-mediated mRNA decay factor, regulates cyst wall protein transcripts in Giardia lamblia. PLoS One 3: e3609.
16. Nageshan RK, Roy N, Hehl AB, Tatu U, (2011) Post-transcriptional repair of a split heat shock protein 90 gene by mRNA trans-splicing. J Biol Chem 286: 7116-7122.
17. Roy SW, Hudson AJ, Joseph J, Yee J, Russell AG, (2011) Numerous fragmented spliceosomal introns, AT-AC splicing, and an unusual dynein gene expression pathway in Giardia lamblia. Mol Biol Evol doi: 10.1093/molbev/msr063.
18. Kamikawa R, Inagaki Y, Tokoro M, Roger AJ, Hashimoto T, (2011) Split introns in the genome of Giardia intestinalis are excised by spliceosome-mediated trans-splicing. Curr Biol 21: 311-315.
19. Russell AG, Shutt TE, Watkins RF, Gray MW, (2005) An ancient spliceosomal intron in the ribosomal protein L7a gene (Rpl7a) of Giardia lamblia. BMC Evol Biol 5: 45.
20. Nixon JE, Wang A, Morrison HG, McArthur AG, Sogin ML, et al. (2002) A spliceosomal intron in Giardia lamblia. Proc Natl Acad Sci U S A 99: 3701-3705.
21. Prucca CG, Slavin I, Quiroga R, Elias EV, Rivero FD, et al. (2008) Antigenic variation in Giardia lamblia is regulated by RNA interference. Nature 456: 750-754.
22. Saraiya AA, Wang CC, (2008) snoRNA, a novel precursor of microRNA in Giardia lamblia. PLoS Pathog 4: e1000224.
23. Li W, Saraiya AA, Wang CC, (2011) Gene Regulation in Giardia lambia Involves a Putative MicroRNA Derived from a Small Nucleolar RNA. PLoS Negl Trop Dis 5: e1338.
24. Birkeland SR, Preheim SP, Davids BJ, Cipriano MJ, Palm D, et al. (2010) Transcriptome analyses of the Giardia lamblia life cycle. Mol Biochem Parasitol 174: 62-65.
25. Muller J, Ley S, Felger I, Hemphill A, Muller N, (2008) Identification of differentially expressed genes in a Giardia lamblia WB C6 clone resistant to nitazoxanide and metronidazole. J Antimicrob Chemother 62: 72-82.
26. Ringqvist E, Avesson L, Soderbom F, Svard SG, (2011) Transcriptional changes in Giardia during host-parasite interactions. Int J Parasitol 41: 277-285.
27. Roxstrom-Lindquist K, Ringqvist E, Palm D, Svard S, (2005) Giardia lamblia-induced changes in gene expression in differentiated Caco-2 human intestinal epithelial cells. Infect Immun 73: 8204-8208.
28. Sonda S, Morf L, Bottova I, Baetschmann H, Rehrauer H, et al. (2010) Epigenetic mechanisms regulate stage differentiation in the minimized protozoan Giardia lamblia. Mol Microbiol 76: 48-67.
29. Morf L, Spycher C, Rehrauer H, Fournier CA, Morrison HG, et al. (2010) The transcriptional response to encystation stimuli in Giardia lamblia is restricted to a small set of genes. Eukaryot Cell 9: 1566-1576.
30. Teodorovic S, Walls CD, Elmendorf HG, (2007) Bidirectional transcription is an inherent feature of Giardia lamblia promoters and contributes to an abundance of sterile antisense transcripts throughout the genome. Nucleic Acids Res 35: 2544-2553.
31. Barrett T, Troup DB, Wilhite SE, Ledoux P, Evangelista C, et al. (2011) NCBI GEO: archive for functional genomics data sets-10 years on. Nucleic Acids Res 39: D1005-1010.
32. Aurrecoechea C, Brestelli J, Brunk BP, Carlton JM, Dommer J, et al. (2009) GiardiaDB and TrichDB: integrated genomic resources for the eukaryotic protist pathogens Giardia lamblia and Trichomonas vaginalis. Nucleic Acids Res 37: D526-530.
33. Smith PD, Gillin FD, Spira WM, Nash TE, (1982) Chronic giardiasis: studies on drug sensitivity, toxin production, and host immune response. Gastroenterology 83: 797-803.
34. Aggarwal A, Merritt JW Jr, Nash TE, (1989) Cysteine-rich variant surface proteins of Giardia lamblia. Mol Biochem Parasitol 32: 39-47.
35. Koudela B, Nohynkova E, Vitovec J, Pakandl M, Kulda J, (1991) Giardia infection in pigs: detection and in vitro isolation of trophozoites of the Giardia intestinalis group. Parasitology 102 Pt 2: 163-166.
36. Ankarklev J (2012) Inter and Intra-Assemblage Characterizations of Giardia intestinalis: from clinic to genome (doctoral thesis). Uppsala: Uppsala University.
37. Roxstrom-Lindquist K, Jerlstrom-Hultqvist J, Jorgensen A, Troell K, Svard SG, et al. (2010) Large genomic differences between the morphologically indistinguishable diplomonads Spironucleus barkhanus and Spironucleus salmonicida. BMC Genomics 11: 258.
38. Lechner M, Findeiss S, Steiner L, Marz M, Stadler PF, et al. (2011) Proteinortho: detection of (co-)orthologs in large-scale analysis. BMC Bioinformatics 12: 124.
39. Langmead B, Salzberg SL, (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
40. Roberts A, Pimentel H, Trapnell C, Pachter L, (2011) Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics 27: 2325-2329.
41. Schmidt HA, von Haeseler A, (2007) Maximum-likelihood analysis using TREE-PUZZLE. Curr Protoc Bioinformatics 17: 6.6.1-6.6.23.
42. Petersen TN, Brunak S, von Heijne G, Nielsen H, (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
43. Krogh A, Larsson B, von Heijne G, Sonnhammer EL, (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
44. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
45. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-208.
46. Beaudoing E, Freier S, Wyatt JR, Claverie JM, Gautheret D, (2000) Patterns of variant polyadenylation signal usage in human genes. Genome Res 10: 1001-1010.
47. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
48. Hu X, Yuan J, Shi Y, Lu J, Liu B, et al. (2012) pIRS: Profile-based Illumina pair-end reads simulator. Bioinformatics 28: 1533-1535.
49. Trapnell C, Pachter L, Salzberg SL, (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
50. Garber M, Grabherr MG, Guttman M, Trapnell C, (2011) Computational methods for transcriptome annotation and quantification using RNA-seq. Nat Methods 8: 469-477.
51. Hansen KD, Brenner SE, Dudoit S, (2010) Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucleic Acids Res 38: e131.
52. Busby MA, Gray JM, Costa AM, Stewart C, Stromberg MP, et al. (2011) Expression divergence measured by transcriptome sequencing of four yeast species. BMC Genomics 12: 635.
53. Saraiya AA, Li W, Wang CC, (2011) A microRNA derived from an apparent canonical biogenesis pathway regulates variant surface protein gene expression in Giardia lamblia. RNA 17: 2152-2164.
54. Li L, Wang CC, (2004) Capped mRNA with a single nucleotide leader is optimally translated in a primitive eukaryote, Giardia lamblia. J Biol Chem 279: 14656-14664.
55. Adam RD, (2001) Biology of Giardia lamblia. Clin Microbiol Rev 14: 447-475.
56. Fabian MR, Sonenberg N, Filipowicz W, (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79: 351-379.
57. Pauws E, van Kampen AH, van de Graaf SA, de Vijlder JJ, Ris-Stalpers C, (2001) Heterogeneity in polyadenylation cleavage sites in mammalian mRNA sequences: implications for SAGE analysis. Nucleic Acids Res 29: 1690-1694.
58. Wu X, Liu M, Downie B, Liang C, Ji G, et al. (2011) Genome-wide landscape of polyadenylation in Arabidopsis provides evidence for extensive alternative polyadenylation. Proc Natl Acad Sci U S A 108: 12533-12538.
59. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, et al. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320: 1344-1349.
60. Mok MT, Tay E, Sekyere E, Glenn WK, Bagnara AS, et al. (2005) Giardia intestinalis: molecular characterization of UDP-N-acetylglucosamine pyrophosphorylase. Gene 357: 73-82.
61. Que X, Svard SG, Meng TC, Hetsko ML, Aley SB, et al. (1996) Developmentally regulated transcripts and evidence of differential mRNA processing in Giardia lamblia. Mol Biochem Parasitol 81: 101-110.
62. Svard SG, Rafferty C, McCaffery JM, Smith MW, Reiner DS, et al. (1999) A signal recognition particle receptor gene from the early-diverging eukaryote, Giardia lamblia. Mol Biochem Parasitol 98: 253-264.
63. Skarin H, Ringqvist E, Hellman U, Svard SG, (2011) Elongation factor 1-alpha is released into the culture medium during growth of Giardia intestinalis trophozoites. Exp Parasitol 127: 804-810.
64. Adam RD, Nigam A, Seshadri V, Martens CA, Farneth GA, et al. (2010) The Giardia lamblia vsp gene repertoire: characteristics, genomic organization, and evolution. BMC Genomics 11: 424.
65. Nash TE, Lujan HT, Mowatt MR, Conrad JT, (2001) Variant-specific surface protein switching in Giardia lamblia. Infect Immun 69: 1922-1923.
66. Ankarklev J, Svard SG, Lebbad M, (2012) Allelic sequence heterozygosity in single Giardia parasites. BMC Microbiol 12: 65.
67. Vijaya Satya R, Zavaljevski N, Reifman J, (2012) A new strategy to reduce allelic bias in RNA-Seq readmapping. Nucleic Acids Res 40: e127.
68. Degner JF, Marioni JC, Pai AA, Pickrell JK, Nkadori E, et al. (2009) Effect of read-mapping biases on detecting allele-specific expression from RNA-sequencing data. Bioinformatics 25: 3207-3212.
69. DeVeale B, van der Kooy D, Babak T, (2012) Critical evaluation of imprinted gene expression by RNA-Seq: a new perspective. PLoS Genet 8: e1002600.
70. Jeffares DC, Mourier T, Penny D, (2006) The biology of intron gain and loss. Trends Genet 22: 16-22.
71. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.