Genome wide distribution of G-quadruplexes and their impact on gene expression in malaria parasites
Autoři:
Elodie Gazanion aff001; Laurent Lacroix aff002; Patrizia Alberti aff003; Pratima Gurung aff004; Sharon Wein aff004; Mingpan Cheng aff005; Jean-Louis Mergny aff005; Ana Rita Gomes aff004; Jose-Juan Lopez-Rubio aff001
Působiště autorů:
MIVEGEC UMR IRD 224, CNRS 5290, Montpellier University, Montpellier, France
aff001; IBENS, Ecole Normale Supérieure, CNRS, Inserm, PSL Research University, Paris, France
aff002; "Structure and Instability of Genomes" laboratory, Muséum National d'Histoire Naturelle (MNHN), Inserm U1154, CNRS UMR 7196, Paris, France
aff003; Laboratory of Pathogen-Host Interactions (LPHI), UMR5235, CNRS, Montpellier University, Montpellier, France
aff004; ARNA Laboratory, IECB, CNRS UMR5320, INSERM U1212, Bordeaux University, Pessac, France
aff005; Institute of Biophysics of the Czech Academy of Sciences, Czech Republic
aff006; Laboratoire d’Optique et Biosciences, Ecole Polytechnique, CNRS, INSERM, Institut Polytechnique de Paris, France
aff007
Vyšlo v časopise:
Genome wide distribution of G-quadruplexes and their impact on gene expression in malaria parasites. PLoS Genet 16(7): e32767. doi:10.1371/journal.pgen.1008917
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008917
Souhrn
Mechanisms of transcriptional control in malaria parasites are still not fully understood. The positioning patterns of G-quadruplex (G4) DNA motifs in the parasite’s AT-rich genome, especially within the var gene family which encodes virulence factors, and in the vicinity of recombination hotspots, points towards a possible regulatory role of G4 in gene expression and genome stability. Here, we carried out the most comprehensive genome-wide survey, to date, of G4s in the Plasmodium falciparum genome using G4Hunter, which identifies G4 forming sequences (G4FS) considering their G-richness and G-skewness. We show an enrichment of G4FS in nucleosome-depleted regions and in the first exon of var genes, a pattern that is conserved within the closely related Laverania Plasmodium parasites. Under G4-stabilizing conditions, i.e., following treatment with pyridostatin (a high affinity G4 ligand), we show that a bona fide G4 found in the non-coding strand of var promoters modulates reporter gene expression. Furthermore, transcriptional profiling of pyridostatin-treated parasites, shows large scale perturbations, with deregulation affecting for instance the ApiAP2 family of transcription factors and genes involved in ribosome biogenesis. Overall, our study highlights G4s as important DNA secondary structures with a role in Plasmodium gene expression regulation, sub-telomeric recombination and var gene biology.
Klíčová slova:
Gene expression – Gene regulation – Genome analysis – Introns – Malarial parasites – Plasmodium – Plasmodium falciparum – Sequence motif analysis
Zdroje
1. WHO. World malaria report 2018. WHO website. 2018. http://www.who.int/malaria/publications/world-malaria-report-2018/report/en/
2. Bozdech Z, Llinás M, Pulliam BL, Wong ED, Zhu J, DeRisi JL. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 2003;1: E5. doi: 10.1371/journal.pbio.0000005 12929205
3. van Noort V, Huynen MA. Combinatorial gene regulation in Plasmodium falciparum. Trends Genet. 2006;22: 73–8. doi: 10.1016/j.tig.2005.12.002 16380193
4. Scherf A, Lopez-Rubio JJ, Riviere L. Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol. 2008;62: 445–470. doi: 10.1146/annurev.micro.61.080706.093134 18785843
5. Kraemer SM, Kyes SA, Aggarwal G, Springer AL, Nelson SO, Christodoulou Z, et al. Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates. BMC Genomics. 2007;8: 45. doi: 10.1186/1471-2164-8-45 17286864
6. Jiang L, Mu J, Zhang Q, Ni T, Srinivasan P, Rayavara K, et al. PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature. 2013;499: 223–227. doi: 10.1038/nature12361 23823717
7. Lopez-Rubio J-J, Mancio-Silva L, Scherf A. Genome-wide analysis of heterochromatin associates clonally variant gene regulation with perinuclear repressive centers in malaria parasites. Cell Host Microbe. 2009;5: 179–190. doi: 10.1016/j.chom.2008.12.012 19218088
8. Wang C, Adapa SR, Gibbons J, Sutton S, Jiang RHY. Punctuated chromatin states regulate Plasmodium falciparum antigenic variation at the intron and 2 kb upstream regions. BMC Genomics. 2016;17: 652. doi: 10.1186/s12864-016-3005-7 27538502
9. Amit-Avraham I, Pozner G, Eshar S, Fastman Y, Kolevzon N, Yavin E, et al. Antisense long noncoding RNAs regulate var gene activation in the malaria parasite Plasmodium falciparum. Proc Natl Acad Sci. 2015;112: E982–E991. doi: 10.1073/pnas.1420855112 25691743
10. Rowe JA, Claessens A, Corrigan RA, Arman M. Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Rev Mol Med. 2009;11: e16. doi: 10.1017/S1462399409001082 19467172
11. Bochman ML, Paeschke K, Zakian VA. DNA secondary structures: stability and function of G-quadruplex structures. Nat Rev Genet. 2012;13: 770–780. doi: 10.1038/nrg3296 23032257
12. Maizels N. Dynamic roles for G4 DNA in the biology of eukaryotic cells. Nat Struct Mol Biol. 2006;13: 1055–1059. doi: 10.1038/nsmb1171 17146462
13. Maizels N, Gray LT. The G4 genome. PLoS Genet. 2013;9: e1003468. doi: 10.1371/journal.pgen.1003468 23637633
14. Hänsel-Hertsch R, Beraldi D, Lensing S V, Marsico G, Zyner K, Parry A, et al. G-quadruplex structures mark human regulatory chromatin. Nat Genet. 2016;48: 1267–1272. doi: 10.1038/ng.3662 27618450
15. Hänsel-Hertsch R, Di Antonio M, Balasubramanian S. DNA G-quadruplexes in the human genome: Detection, functions and therapeutic potential. Nat Rev Mol Cell Biol. 2017;18: 279–284. doi: 10.1038/nrm.2017.3 28225080
16. Rodriguez R, Miller KM, Forment J V, Bradshaw CR, Nikan M, Britton S, et al. Small-molecule-induced DNA damage identifies alternative DNA structures in human genes. Nat Chem Biol. 2012;8: 301–310. doi: 10.1038/nchembio.780 22306580
17. Siddiqui-Jain A, Grand CL, Bearss DJ, Hurley LH. Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc Natl Acad Sci. 2002;99: 11593–11598. doi: 10.1073/pnas.182256799 12195017
18. Zaug AJ, Podell ER, Cech TR. Human POT1 disrupts telomeric G-quadruplexes allowing telomerase extension in vitro. Proc Natl Acad Sci. 2005;102: 10864–10869. doi: 10.1073/pnas.0504744102 16043710
19. Shahid R, Bugaut A, Balasubramanian S. The BCL-2 5′ untranslated region contains an RNA G-quadruplex-forming motif that modulates protein expression. Biochemistry. 2010;49: 8300–8306. doi: 10.1021/bi100957h 20726580
20. Balasubramanian S, Hurley LH, Neidle S. Targeting G-quadruplexes in gene promoters: a novel anticancer strategy? Nat Rev Drug Discov. 2011;10: 261–275. doi: 10.1038/nrd3428 21455236
21. Neidle S. Quadruplex Nucleic Acids as Novel Therapeutic Targets. J Med Chem. 2016;59: 5987–6011. doi: 10.1021/acs.jmedchem.5b01835 26840940
22. Drygin D, Siddiqui-Jain A, O’Brien S, Schwaebe M, Lin A, Bliesath J, et al. Anticancer activity of CX-3543: A direct inhibitor of rRNA biogenesis. Cancer Res. 2009;69: 7653–7661. doi: 10.1158/0008-5472.CAN-09-1304 19738048
23. Capra JA, Paeschke K, Singh M, Zakian VA. G-quadruplex DNA sequences are evolutionarily conserved and associated with distinct genomic features in Saccharomyces cerevisiae. PLoS Comput Biol. 2010;6: e1000861. doi: 10.1371/journal.pcbi.1000861 20676380
24. Rawal P, Kummarasetti VB, Ravindran J, Kumar N, Halder K, Sharma R, et al. Genome-wide prediction of G4 DNA as regulatory motifs: role in Escherichia coli global regulation. Genome Res. 2006;16: 644–655. doi: 10.1101/gr.4508806 16651665
25. Perrone R, Lavezzo E, Riello E, Manganelli R, Palu G, Toppo S, et al. Mapping and characterization of G-quadruplexes in Mycobacterium tuberculosis gene promoter regions. Sci Rep. 2017;7: 5743. doi: 10.1038/s41598-017-05867-z 28720801
26. Garg R, Aggarwal J, Thakkar B. Genome-wide discovery of G-quadruplex forming sequences and their functional relevance in plants. Sci Rep. 2016;6: 28211. doi: 10.1038/srep28211 27324275
27. Lavezzo E, Berselli M, Frasson I, Perrone R, Palù G, Brazzale AR, et al. G-quadruplex forming sequences in the genome of all known human viruses: A comprehensive guide. PLoS Comput Biol. 2018;14: e1006675. doi: 10.1371/journal.pcbi.1006675 30543627
28. Belmonte-Reche E, Martinez-Garcia M, Guedin A, Zuffo M, Arevalo-Ruiz M, Doria F, et al. G-Quadruplex Identification in the Genome of Protozoan Parasites Points to Naphthalene Diimide Ligands as New Antiparasitic Agents. J Med Chem. 2018;61: 1231–1240. doi: 10.1021/acs.jmedchem.7b01672 29323491
29. Smargiasso N, Gabelica V, Damblon C, Rosu F, De Pauw E, Teulade-Fichou MP, et al. Putative DNA G-quadruplex formation within the promoters of Plasmodium falciparum var genes. BMC Genomics. 2009;10: 362. doi: 10.1186/1471-2164-10-362 19660104
30. Chambers VS, Marsico G, Boutell JM, Di Antonio M, Smith GP, Balasubramanian S. High-throughput sequencing of DNA G-quadruplex structures in the human genome. Nat Biotechnol. 2015;33: 877–881. doi: 10.1038/nbt.3295 26192317
31. Marsico G, Chambers VS, Sahakyan AB, McCauley P, Boutell JM, Di Antonio M, et al. Whole genome experimental maps of DNA G-quadruplexes in multiple species. Nucleic Acids Res. 2019;47: 3862–3874. doi: 10.1093/nar/gkz179 30892612
32. Cahoon LA, Seifert HS. An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science (80-). 2009;325: 764–767. doi: 10.1126/science.1175653 19661435
33. Perrone R, Nadai M, Frasson I, Poe JA, Butovskaya E, Smithgall TE, et al. A Dynamic G-quadruplex region regulates the HIV-1 Long terminal repeat promoter. J Med Chem. 2013;56: 6521–6530. doi: 10.1021/jm400914r 23865750
34. Murat P, Zhong J, Lekieffre L, Cowieson NP, Clancy JL, Preiss T, et al. G-quadruplexes regulate Epstein-Barr virus-encoded nuclear antigen 1 mRNA translation. Nat Chem Biol. 2014;10: 358–364. doi: 10.1038/nchembio.1479 24633353
35. Biswas B, Kandpal M, Jauhari UK, Vivekanandan P. Genome-wide analysis of G-quadruplexes in herpesvirus genomes. BMC Genomics. 2016;17: 949. doi: 10.1186/s12864-016-3282-1 27871228
36. Harris LM, Monsell KR, Noulin F, Toyin Famodimu M, Smargiasso N, Damblon C, et al. G-quadruplex DNA motifs in the malaria parasite Plasmodium falciparum and their potential as novel antimalarial drug targets. Antimicrob Agents Chemother. 2018;62: e01828–17. doi: 10.1128/AAC.01828-17 29311059
37. Anas M, Sharma R, Dhamodharan V, Pradeepkumar PI, Manhas A, Srivastava K, et al. Investigating Pharmacological Targeting of G-Quadruplexes in the Human Malaria Parasite. Biochemistry. 2017;56: 6691–6699. doi: 10.1021/acs.biochem.7b00964 29182860
38. Guillon J, Cohen A, Das RN, Boudot C, Gueddouda NM, Moreau S, et al. Design, synthesis, and antiprotozoal evaluation of new 2,9-bis[(substituted-aminomethyl)phenyl]-1,10-phenanthroline derivatives. Chem Biol Drug Des. 2018;91: 974–995. doi: 10.1111/cbdd.13164 29266861
39. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature. 2002;19: 498–511. doi: 10.1038/nature01097 12368864
40. Stanton A, Harris LM, Graham G, Merrick CJ. Recombination events among virulence genes in malaria parasites are associated with G-quadruplex-forming DNA motifs. BMC Genomics. 2016;17: 859. doi: 10.1186/s12864-016-3183-3 27809775
41. Bedrat A, Lacroix L, Mergny JL. Re-evaluation of G-quadruplex propensity with G4Hunter. Nucleic Acids Res. 2016;44: 1746–1759. doi: 10.1093/nar/gkw006 26792894
42. Claessens A, Harris LM, Stanojcic S, Chappell L, Stanton A, Kuk N, et al. RecQ helicases in the malaria parasite Plasmodium falciparum affect genome stability, gene expression patterns and DNA replication dynamics. PLoS Genet. 2018;14: e1007490. doi: 10.1371/journal.pgen.1007490 29965959
43. Bhartiya D, Chawla V, Ghosh S, Shankar R, Kumar N. Genome-wide regulatory dynamics of G-quadruplexes in human malaria parasite Plasmodium falciparum. Genomics. 2016;108: 224–231. doi: 10.1016/j.ygeno.2016.10.004 27789319
44. Huppert JL, Balasubramanian S. Prevalence of quadruplexes in the human genome. Nucleic Acids Res. 2005;33: 2908–2916. doi: 10.1093/nar/gki609 15914667
45. Kikin O, D’Antonio L, Bagga PS. QGRS Mapper: a web-based server for predicting G-quadruplexes in nucleotide sequences. Nucleic Acids Res. 2006;34: W676–W682. doi: 10.1093/nar/gkl253 16845096
46. Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, et al. PlasmoDB: A functional genomic database for malaria parasites. Nucleic Acids Res. 2009;37: D539–543. doi: 10.1093/nar/gkn814 18957442
47. Saad M, Guédin A, Amor S, Bedrat A, Tourasse NJ, Fayyad-Kazan H, et al. Mapping and characterization of G-quadruplexes in the genome of the social amoeba Dictyostelium discoideum. Nucleic Acids Res. 2019;47: 4363–4374. doi: 10.1093/nar/gkz196 30923812
48. Guédin A, Lin LY, Armane S, Lacroix L, Mergny J-L, Thore S, et al. Quadruplexes in ‘Dicty’: crystal structure of a four-quartet G-quadruplex formed by G-rich motif found in the Dictyostelium discoideum genome. Nucleic Acids Res. 2018;46: 5297–5307. doi: 10.1093/nar/gky290 29718337
49. Ruiz JL, Tena JJ, Bancells C, Cortés A, Gómez-Skarmeta JL, Gómez-Díaz E. Characterization of the accessible genome in the human malaria parasite Plasmodium falciparum. Nucleic Acids Res. 2018;46: 9414–9431. doi: 10.1093/nar/gky643 30016465
50. Adjalley SH, Chabbert CD, Klaus B, Pelechano V, Steinmetz LM. Landscape and Dynamics of Transcription Initiation in the Malaria Parasite Plasmodium falciparum. Cell Rep. 2016;14: 2463–2475. doi: 10.1016/j.celrep.2016.02.025 26947071
51. Calvo EP, Wasserman M. G-Quadruplex ligands: Potent inhibitors of telomerase activity and cell proliferation in Plasmodium falciparum. Mol Biochem Parasitol. 2016;207: 33–38. doi: 10.1016/j.molbiopara.2016.05.009 27217226
52. De Cian A, Grellier P, Mouray E, Depoix D, Bertrand H, Monchaud D, et al. Plasmodium telomeric sequences: structure, stability and quadruplex targeting by small compounds. Chembiochem. 2008;9: 2730–9. doi: 10.1002/cbic.200800330 18924216
53. Rask TS, Hansen DA, Theander TG, Pedersen AG, Lavstsen T. Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes—divide and conquer. PLoS Comput Biol. 2010;6. doi: 10.1371/journal.pcbi.1000933 20862303
54. Otto TD, Gilabert A, Crellen T, Böhme U, Arnathau C, Sanders M, et al. Genomes of all known members of a Plasmodium subgenus reveal paths to virulent human malaria. Nat Microbiol. 2018;3: 687–697. doi: 10.1038/s41564-018-0162-2 29784978
55. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, et al. MEME Suite: Tools for motif discovery and searching. Nucleic Acids Res. 2009;37: W202–W208. doi: 10.1093/nar/gkp335 19458158
56. Ribeyre C, Lopes J, Boulé J-B, Piazza A, Guédin A, Zakian VA, et al. The Yeast Pif1 Helicase Prevents Genomic Instability Caused by G-Quadruplex-Forming CEB1 Sequences In Vivo. Cohen-Fix O, editor. PLoS Genet. 2009;5: e1000475. doi: 10.1371/journal.pgen.1000475 19424434
57. del Villar-Guerra R, Trent JO, Chaires JB. G-Quadruplex Secondary Structure Obtained from Circular Dichroism Spectroscopy. Angew Chemie—Int Ed. 2018;57: 7171–7175. doi: 10.1002/anie.201709184 29076232
58. Mergny JL, Li J, Lacroix L, Amrane S, Chaires JB. Thermal difference spectra: A specific signature for nucleic acid structures. Nucleic Acids Res. 2005;33: e138. doi: 10.1093/nar/gni134 16157860
59. De La Faverie AR, Guédin A, Bedrat A, Yatsunyk LA, Mergny JL. Thioflavin T as a fluorescence light-up probe for G4 formation. Nucleic Acids Res. 2014;42: e65. doi: 10.1093/nar/gku111 24510097
60. Lam EY, Beraldi D, Tannahill D, Balasubramanian S. G-quadruplex structures are stable and detectable in human genomic DNA. Nat Commun. 2013;4: 1796. doi: 10.1038/ncomms2792 23653208
61. Frank M, Deitsch K. Activation, silencing and mutually exclusive expression within the var gene family of Plasmodium falciparum. Int J Parasitol. 2006;36: 975–985. doi: 10.1016/j.ijpara.2006.05.007 16797552
62. Desjardins RE, Canfield CJ, Haynes JD, Chulay JD. Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob Agents Chemother. 1979;16: 710–8. doi: 10.1128/aac.16.6.710 394674
63. Painter HJ, Campbell TL, Llinás M. The Apicomplexan AP2 family: integral factors regulating Plasmodium development. Mol Biochem Parasitol. 2011;176: 1–7. doi: 10.1016/j.molbiopara.2010.11.014 21126543
64. Eddy J, Maizels N. Conserved elements with potential to form polymorphic G-quadruplex structures in the first intron of human genes. Nucleic Acids Res. 2008;36: 1321–33. doi: 10.1093/nar/gkm1138 18187510
65. Huppert JL, Balasubramanian S. G-quadruplexes in promoters throughout the human genome. Nucleic Acids Res. 2007. doi: 10.1093/nar/gkl1057 17169996
66. Smestad JA, Maher LJ. Relationships between putative G-quadruplex-forming sequences, RecQ helicases, and transcription. BMC Med Genet. 2015;16: 91. doi: 10.1186/s12881-015-0236-4 26449372
67. Huppert JL, Bugaut A, Kumari S, Balasubramanian S. G-quadruplexes: the beginning and end of UTRs. Nucleic Acids Res. 2008;36: 6260–6268. doi: 10.1093/nar/gkn511 18832370
68. Claessens A, Hamilton WL, Kekre M, Otto TD, Faizullabhoy A, Rayner JC, et al. Generation of Antigenic Diversity in Plasmodium falciparum by Structured Rearrangement of Var Genes During Mitosis. PLoS Genet. 2014;10: e1004812. doi: 10.1371/journal.pgen.1004812 25521112
69. Bopp SER, Manary MJ, Bright AT, Johnston GL, Dharia N V., Luna FL, et al. Mitotic Evolution of Plasmodium falciparum Shows a Stable Core Genome but Recombination in Antigen Families. PLoS Genet. 2013;9: e1003293. doi: 10.1371/journal.pgen.1003293 23408914
70. Verma A, Yadav VK, Basundra R, Kumar A, Chowdhury S. Evidence of genome-wide G4 DNA-mediated gene expression in human cancer cells. Nucleic Acids Res. 2009;37: 4194–4204. doi: 10.1093/nar/gkn1076 19211664
71. Halder R, Riou JF, Teulade-Fichou MP, Frickey T, Hartig JS. Bisquinolinium compounds induce quadruplex-specific transcriptome changes in HeLa S3 cell lines. BMC Res Notes. 2012;5: 138. doi: 10.1186/1756-0500-5-138 22414013
72. Lawrence M, Huber W, Pagès H, Aboyoun P, Carlson M, Gentleman R, et al. Software for Computing and Annotating Genomic Ranges. Prlic A, editor. PLoS Comput Biol. 2013;9: e1003118. doi: 10.1371/journal.pcbi.1003118 23950696
73. Lawrence M, Gentleman R, Carey V. rtracklayer: an R package for interfacing with genome browsers. Bioinformatics. 2009;25: 1841–1842. doi: 10.1093/bioinformatics/btp328 19468054
74. Kensche PR, Hoeijmakers WAM, Toenhake CG, Bras M, Chappell L, Berriman M, et al. The nucleosome landscape of Plasmodium falciparum reveals chromatin architecture and dynamics of regulatory sequences. Nucleic Acids Res. 2015;44: 2110–2124. doi: 10.1093/nar/gkv1214 26578577
75. Sims D, Ilott NE, Sansom SN, Sudbery IM, Johnson JS, Fawcett KA, et al. CGAT: Computational genomics analysis toolkit. Bioinformatics. 2014;30: 1290–1291. doi: 10.1093/bioinformatics/btt756 24395753
76. Lelièvre J, Berry A, Benoit-Vical F. An alternative method for Plasmodium culture synchronization. Exp Parasitol. 2005;109: 195–197. doi: 10.1016/j.exppara.2004.11.012 15713452
77. Lambros C, Vanderberg JP. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol. 1979;65: 418–20. Available: http://www.ncbi.nlm.nih.gov/pubmed/383936 383936
78. Wu Y, Sifri CD, Lei HH, Su XZ, Wellems TE. Transfection of Plasmodium falciparum within human red blood cells. Proc Natl Acad Sci U S A. 1995;92: 973–7. doi: 10.1073/pnas.92.4.973 7862676
79. Epp C, Li F, Howitt CA, Chookajorn T, Deitsch KW. Chromatin associated sense and antisense noncoding RNAs are transcribed from the var gene family of virulence genes of the malaria parasite Plasmodium falciparum. RNA. 2009;15: 116–27. doi: 10.1261/rna.1080109 19037012
80. Salanti A, Staalsoe T, Lavstsen T, Jensen ATR, Sowa MPK, Arnot DE, et al. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol. 2003;49: 179–191. doi: 10.1046/j.1365-2958.2003.03570.x 12823820
81. Dzikowski R, Frank M, Deitsch K. Mutually Exclusive Expression of Virulence Genes by Malaria Parasites Is Regulated Independently of Antigen Production. PLoS Pathog. 2006;2: e22. doi: 10.1371/journal.ppat.0020022 16518466
82. Siegel TN, Hon CC, Zhang Q, Lopez-Rubio JJ, Scheidig-Benatar C, Martins RM, et al. Strand-specific RNA-Seq reveals widespread and developmentally regulated transcription of natural antisense transcripts in Plasmodium falciparum. BMC Genomics. 2014;15: 150. doi: 10.1186/1471-2164-15-150 24559473
83. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168
84. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15: 550. doi: 10.1186/s13059-014-0550-8 25516281
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 7
- Případ Bulovka: Jak postupují jiné nemocnice, aby podobným tragédiím zabránily?
- Jak často se u masových střelců vyskytují duševní choroby?
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Není statin jako statin aneb praktický přehled rozdílů jednotlivých molekul
Nejčtenější v tomto čísle
- Holocentric chromosomes
- Repression of tick microRNA-133 induces organic anion transporting polypeptide expression critical for Anaplasma phagocytophilum survival in the vector and transmission to the vertebrate host
- Brassinosteroids regulate root meristem development by mediating BIN2-UPB1 module in Arabidopsis
- Genetic and metabolomic architecture of variation in diet restriction-mediated lifespan extension in Drosophila