Diversity and expression of microRNAs in the filarial parasite, Brugia malayi

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Poole, Catherine B ^a,b   Gu, Weifeng ^c   Kumar, Sanjay ^b   Jin, Jingmin ^a   Davis, Paul J ^b   Bauche, David ^a,d   McReynolds, Larry A ^a,b  

^a New England Biolabs   (United States)

^b Division of Molecular Parasitology   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; P19 RNA BINDING PROTEIN; RNA; RNA BINDING PROTEIN; SMALL RNA; UNCLASSIFIED DRUG;

ARTHROPOD; ARTICLE; BRUGIA MALAYI; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENETIC CONSERVATION; GENETIC VARIABILITY; GENOME ANALYSIS; HELMINTH; MALE; MICROFILARIA (NEMATODE LARVA); MOLECULAR CLONING; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; VERTEBRATE; ANIMAL; GENE LIBRARY; GENETICS; GENOME;

ANIMALS; BRUGIA MALAYI; GENE LIBRARY; GENOME, HELMINTH; MICRORNAS;

EID: 84901263109     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096498     Document Type: Article

References (75)

1. WHO (1992) Lymphatic filariasis: the disease and its control. Fifth report of the WHO Expert Committee on Filariasis. 0512-3054 (Print)0512-3054 (Linking). 1-71 p.
2. Scott AL (2000) Lymphatic-dwelling Filariae. In: Nutman TB, editor. Lymphatic Filariasis. London: Imperial College Press. pp. 5-40.
3. Simonsen PE (2009) Filariases. In: Cook G, Manson P, Zumla A, editors. Manson's Tropical Diseases. 22 ed: Saunders, Elsevier. pp. 1477-1513.
4. Kumaraswami V (2000) The Clinical Manifestations of Lymphatic Filariasis. In: Nutman TB, editor. Lymphatic Filariasis. London: Imperial College Press. pp. 103-126.
5. Molyneux DH, Taylor MJ (2001) Current status and future prospects of the Global Lymphatic Filariasis Programme. Curr Opin Infect Dis 14: 155-159. (Pubitemid 32231102)
6. Addiss DG, Dreyer G (2000) Treatment of Lymphatic Filariasis. In: Nutman TB, editor. Lymphatic Filariasis. London: Imperial College Press. pp. 151-200.
7. Bourguinat C, Ardelli BF, Pion SD, Kamgno J, Gardon J, et al. (2008) P-glycoprotein-like protein, a possible genetic marker for ivermectin resistance selection in Onchocerca volvulus. Mol Biochem Parasitol 158: 101-111. (Pubitemid 351255520)
8. Williams SA, Lizotte-Waniewski MR, Foster J, Guiliano D, Daub J, et al. (2000) The filarial genome project: analysis of the nuclear, mitochondrial and endosymbiont genomes of Brugia malayi. Int J Parasitol 30: 411-419. (Pubitemid 30145470)
9. Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, et al. (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317: 1756-1760. (Pubitemid 47461841)
10. Desjardins CA, Cerqueira GC, Goldberg JM, Dunning Hotopp JC, Haas BJ, et al. (2013) Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nature genetics 45: 495-500.
11. Godel C, Kumar S, Koutsovoulos G, Ludin P, Nilsson D, et al. (2012) The genome of the heartworm, Dirofilaria immitis, reveals drug and vaccine targets. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 26: 4650-4661.
12. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854. (Pubitemid 24014542)
13. Wightman B, Ha I, Ruvkun G (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75: 855-862. (Pubitemid 24014543)
14. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
15. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
16. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20. (Pubitemid 40094598)
17. Friedman RC, Farh KK, Burge CB, Bartel DP (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome research 19: 92-105.
18. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, et al. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Molecular cell 27: 91-105. (Pubitemid 46991392)
19. Shin C, Nam JW, Farh KK, Chiang HR, Shkumatava A, et al. (2010) Expanding the microRNA targeting code: functional sites with centered pairing. Molecular cell 38: 789-802.
20. Brennecke J, Stark A, Russell RB, Cohen SM (2005) Principles of microRNA-target recognition. PLoS biology 3: e85.
21. Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P, et al. (2006) mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 20: 1885-1898. (Pubitemid 44079326)
22. Eulalio A, Huntzinger E, Izaurralde E (2008) GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat Struct Mol Biol 15: 346-353. (Pubitemid 351483394)
23. Prochnik SE, Rokhsar DS, Aboobaker AA (2007) Evidence for a microRNA expansion in the bilaterian ancestor. Dev Genes Evol 217: 73-77. (Pubitemid 46062716)
24. Wheeler BM, Heimberg AM, Moy VN, Sperling EA, Holstein TW, et al. (2009) The deep evolution of metazoan microRNAs. Evol Dev 11: 50-68.
25. Lau NC, Lim LP, Weinstein EG, Bartel DP (2001) An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294: 858-862. (Pubitemid 33032104)
26. Lim LP, Lau NC, Weinstein EG, Abdelhakim A, Yekta S, et al. (2003) The microRNAs of Caenorhabditis elegans. Genes Dev 17: 991-1008. (Pubitemid 36459452)
27. Ambros V, Lee RC, Lavanway A, Williams PT, Jewell D (2003) MicroRNAs and other tiny endogenous RNAs in C. elegans. Curr Biol 13: 807-818. (Pubitemid 36573248)
28. Grad Y, Aach J, Hayes GD, Reinhart BJ, Church GM, et al. (2003) Computational and experimental identification of C. elegans microRNAs. Mol Cell 11: 1253-1263. (Pubitemid 36645144)
29. Ruby JG, Jan C, Player C, Axtell MJ, Lee W, et al. (2006) Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127: 1193-1207. (Pubitemid 44894525)
30. Kato M, de Lencastre A, Pincus Z, Slack FJ (2009) Dynamic expression of small non-coding RNAs, including novel microRNAs and piRNAs/21U-RNAs, during Caenorhabditis elegans development. Genome Biol 10: R54.
31. Zisoulis DG, Lovci MT, Wilbert ML, Hutt KR, Liang TY, et al. (2010) Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat Struct Mol Biol 17: 173-179.
32. Poole CB, Davis PJ, Jin J, McReynolds LA (2010) Cloning and bioinformatic identification of small RNAs in the filarial nematode, Brugia malayi. Mol Biochem Parasitol 169: 87-94.
33. Winter AD, Weir W, Hunt M, Berriman M, Gilleard JS, et al. (2012) Diversity in parasitic nematode genomes: the microRNAs of Brugia pahangi and Haemonchus contortus are largely novel. BMC Genomics 13: 4.
34. Pak J, Fire A (2007) Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 315: 241-244. (Pubitemid 46166369)
35. Sijen T, Steiner FA, Thijssen KL, Plasterk RH (2007) Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 315: 244-247. (Pubitemid 46166370)
36. Gu W, Shirayama M, Conte D, Jr., Vasale J, Batista PJ, et al. (2009) Distinct argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol Cell 36: 231-244.
37. Basyuk E, Suavet F, Doglio A, Bordonne R, Bertrand E (2003) Human let-7 stem-loop precursors harbor features of RNase III cleavage products. Nucleic Acids Res 31: 6593-6597. (Pubitemid 37508765)
38. Carmell MA, Hannon GJ (2004) RNase III enzymes and the initiation of gene silencing. Nat Struct Mol Biol 11: 214-218. (Pubitemid 38282765)
39. Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, et al. (2003) A uniform system for microRNA annotation. RNA 9: 277-279. (Pubitemid 36246165)
40. Ibanez-Ventoso C, Vora M, Driscoll M (2008) Sequence relationships among C. elegans, D. melanogaster and human microRNAs highlight the extensive conservation of microRNAs in biology. PLoS One 3: e2818.
41. McReynolds LA, DeSimone SM, Williams SA (1986) Cloning and comparison of repeated DNA sequences from the human filarial parasite Brugia malayi and the animal parasite Brugia pahangi. Proc Natl Acad Sci USA 83: 797-801. (Pubitemid 16035562)
42. Friedlander MR, Chen W, Adamidi C, Maaskola J, Einspanier R, et al. (2008) Discovering microRNAs from deep sequencing data using miRDeep. Nat Biotechnol 26: 407-415. (Pubitemid 351501815)
43. Jin J, Cid M, Poole CB, McReynolds LA (2010) Protein mediated miRNA detection and siRNA enrichment using p19. Biotechniques 48: xvii-xxiii.
44. Wanunu M, Dadosh T, Ray V, Jin J, McReynolds L, et al. (2010) Rapid electronic detection of probe-specific microRNAs using thin nanopore sensors. Nature nanotechnology 5: 807-814.
45. Labib M, Khan N, Ghobadloo SM, Cheng J, Pezacki JP, et al. (2013) Three-mode electrochemical sensing of ultralow microRNA levels. Journal of the American Chemical Society 135: 3027-3038.
46. Wang J, Czech B, Crunk A, Wallace A, Mitreva M, et al. (2011) Deep small RNA sequencing from the nematode Ascaris reveals conservation, functional diversification, and novel developmental profiles. Genome research 21: 1462-1477.
47. Sapio MR, Hilliard MA, Cermola M, Favre R, Bazzicalupo P (2005) The Zona Pellucida domain containing proteins, CUT-1, CUT-3 and CUT-5, play essential roles in the development of the larval alae in Caenorhabditis elegans. Dev Biol 282: 231-245. (Pubitemid 40779941)
48. Hussain M, Frentiu FD, Moreira LA, O'Neill SL, Asgari S (2011) Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti. Proc Natl Acad Sci U S A 108: 9250-9255.
49. Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34: D140-144.
50. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36: D154-158. (Pubitemid 351149713)
51. Miska EA, Alvarez-Saavedra E, Abbott AL, Lau NC, Hellman AB, et al. (2007) Most Caenorhabditis elegans microRNAs are individually not essential for development or viability. PLoS Genet 3: e215.
52. Alvarez-Saavedra E, Horvitz HR (2010) Many families of C. elegans microRNAs are not essential for development or viability. Curr Biol 20: 367-373.
53. Leaman D, Chen PY, Fak J, Yalcin A, Pearce M, et al. (2005) Antisense-mediated depletion reveals essential and specific functions of microRNAs in Drosophila development. Cell 121: 1097-1108. (Pubitemid 40884399)
54. Conradt B, Horvitz HR (1998) The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 93: 519-529. (Pubitemid 28240714)
55. Zhang L, Hammell M, Kudlow BA, Ambros V, Han M (2009) Systematic analysis of dynamic miRNA-target interactions during C. elegans development. Development 136: 3043-3055.
56. Hafner M, Renwick N, Brown M, Mihailovic A, Holoch D, et al. (2011) RNA-ligase-dependent biases in miRNA representation in deep-sequenced small RNA cDNA libraries. RNA 17: 1697-1712.
57. Zhuang F, Fuchs RT, Sun Z, Zheng Y, Robb GB (2012) Structural bias in T4 RNA ligase-mediated 39-adapter ligation. Nucleic acids research 40: e54.
58. Isik M, Korswagen HC, Berezikov E (2010) Expression patterns of intronic microRNAs in Caenorhabditis elegans. Silence 1: 5.
59. de Lencastre A, Pincus Z, Zhou K, Kato M, Lee SS, et al. (2010) MicroRNAs both promote and antagonize longevity in C. elegans. Curr Biol 20: 2159-2168.
60. Boulias K, Horvitz HR (2012) The C. elegans microRNA mir-71 acts in neurons to promote germline-mediated longevity through regulation of DAF-16/FOXO. Cell metabolism 15: 439-450.
61. Karp X, Hammell M, Ow MC, Ambros V (2011) Effect of life history on microRNA expression during C. elegans development. RNA 17: 639-651.
62. Ponnudurai T, Denham DA, Rogers R (1975) Studies on Brugia pahangi 9. The longevity of microfilariae transfused from cat to cat. J Helminthol 49: 25-30.
63. Le Bechec A, Portales-Casamar E, Vetter G, Moes M, Zindy PJ, et al. (2011) MIR@NT@N: a framework integrating transcription factors, microRNAs and their targets to identify sub-network motifs in a meta-regulation network model. BMC Bioinformatics 12: 67.
64. Shalgi R, Lieber D, Oren M, Pilpel Y (2007) Global and local architecture of the mammalian microRNA-transcription factor regulatory network. PLoS Comput Biol 3: e131.
65. Martinez NJ, Ow MC, Barrasa MI, Hammell M, Sequerra R, et al. (2008) A C. elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity. Genes Dev 22: 2535-2549.
66. Castanotto D, Rossi JJ (2009) The promises and pitfalls of RNA-interference-based therapeutics. Nature 457: 426-433.
67. Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, et al. (2005) Silencing of microRNAs in vivo with 'antagomirs'. Nature 438: 685-689.
68. Obad S, dos Santos CO, Petri A, Heidenblad M, Broom O, et al. (2011) Silencing of microRNA families by seed-targeting tiny LNAs. Nat Genet 43: 371-378.
69. Weese D, Emde AK, Rausch T, Doring A, Reinert K (2009) RazerS-fast read mapping with sensitivity control. Genome Res 19: 1646-1654.
70. Zhang H, Kolb FA, Jaskiewicz L, Westhof E, Filipowicz W (2004) Single processing center models for human Dicer and bacterial RNase III. Cell 118: 57-68. (Pubitemid 38902814)
71. Cock PJ, Antao T, Chang JT, Chapman BA, Cox CJ, et al. (2009) Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25: 1422-1423.
72. Katoh K, Toh H (2008) Improved accuracy of multiple ncRNA alignment by incorporating structural information into a MAFFT-based framework. BMC Bioinformatics 9: 212.
73. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755. (Pubitemid 32851390)
74. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-469.
75. Shi R, Chiang VL (2005) Facile means for quantifying microRNA expression by real-time PCR. Biotechniques 39: 519-525.