BMC Genomics | |
Long non-coding RNA discovery across the genus anopheles reveals conserved secondary structures within and beyond the Gambiae complex | |
Marc AT Muskavitch1  Robert M Waterhouse2  Adam M Jenkins3  | |
[1] Biogen Idec, 14 Cambridge Center, Cambridge 02142, MA, USA;The Broad Institute of MIT and Harvard, 415 Main Street, Cambridge 02142, MA, USA;Boston College, Chestnut Hill 02467, MA, USA | |
关键词: lncRNA; Malaria; Anopheles; | |
Others : 1177248 DOI : 10.1186/s12864-015-1507-3 |
|
received in 2015-01-09, accepted in 2015-03-30, 发布年份 2015 | |
![]() |
【 摘 要 】
Background
Long non-coding RNAs (lncRNAs) have been defined as mRNA-like transcripts longer than 200 nucleotides that lack significant protein-coding potential, and many of them constitute scaffolds for ribonucleoprotein complexes with critical roles in epigenetic regulation. Various lncRNAs have been implicated in the modulation of chromatin structure, transcriptional and post-transcriptional gene regulation, and regulation of genomic stability in mammals, Caenorhabditis elegans, and Drosophila melanogaster. The purpose of this study is to identify the lncRNA landscape in the malaria vector An. gambiae and assess the evolutionary conservation of lncRNAs and their secondary structures across the Anopheles genus.
Results
Using deep RNA sequencing of multiple Anopheles gambiae life stages, we have identified 2,949 lncRNAs and more than 300 previously unannotated putative protein-coding genes. The lncRNAs exhibit differential expression profiles across life stages and adult genders. We find that across the genus Anopheles, lncRNAs display much lower sequence conservation than protein-coding genes. Additionally, we find that lncRNA secondary structure is highly conserved within the Gambiae complex, but diverges rapidly across the rest of the genus Anopheles.
Conclusions
This study offers one of the first lncRNA secondary structure analyses in vector insects. Our description of lncRNAs in An. gambiae offers the most comprehensive genome-wide insights to date into lncRNAs in this vector mosquito, and defines a set of potential targets for the development of vector-based interventions that may further curb the human malaria burden in disease-endemic countries.
【 授权许可】
2015 Jenkins et al.; licensee BioMed Central.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150429021724454.pdf | 2176KB | ![]() |
|
Figure 6. | 49KB | Image | ![]() |
Figure 5. | 36KB | Image | ![]() |
Figure 4. | 54KB | Image | ![]() |
Figure 3. | 50KB | Image | ![]() |
Figure 2. | 36KB | Image | ![]() |
Figure 1. | 61KB | Image | ![]() |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
【 参考文献 】
- [1]Holt R, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, et al.: The genome sequence of the malaria mosquito Anopheles gambiae. Science 2002, 298:129-49.
- [2]Severson DW, Behura SK: Mosquito genomics: progress and challenges. Annu Rev Entomol 2012, 57:143-66.
- [3]Rund SSC, Hou TY, Ward SM, Collins FH, Duffield GE: Genome-wide profiling of diel and circadian gene expression in the malaria vector Anopheles gambiae. PNAS 2011, 108:E421-30.
- [4]Koutsos AC, Blass C, Meister S, Schmidt S, MacCallum RM, Soares MB, et al.: Life cycle transcriptome of the malaria mosquito Anopheles gambiae and comparison with the fruitfly Drosophila melanogaster. PNAS 2007, 104:11304-9.
- [5]Harker BW, Hong YS, Sim C, Dana AN, Bruggner RV, Lobo NF, et al.: Transcription Profiling Associated with Life Cycles of Anopheles gambiae. J Med Entomol 2012, 49:316-25.
- [6]Edi CV, Djogbénou L, Jenkins AM, Regna K, Muskavitch MAT, Poupardin R, et al.: CYP6 P450 Enzymes and ACE-1 Duplication Produce Extreme and Multiple Insecticide Resistance in the Malaria Mosquito Anopheles gambiae. PLoS Genet 2014., 10Article ID e1004236
- [7]Mitchell SN, Rigden DJ, Dowd AJ, Lu F, Wilding CS, Weetman D, et al.: Metabolic and Target-Site Mechanisms Combine to Confer Strong DDT Resistance in Anopheles gambiae. PLoS One 2014., 9Article ID e92662
- [8]Neira-Oviedo M, Ribeiro JMC, Heyland A, VanEkeris L, Moroz T, Linser PJ: The salivary transcriptome of Anopheles gambiae (Diptera: Culicidae) larvae: A microarray-based analysis. Insect Biochem Mol Biol 2009, 39:382-94.
- [9]Stamboliyska R, Parsch J: Dissecting gene expression in mosquito. BMC Genomics 2011, 12:297. BioMed Central Full Text
- [10]Phuc HK, Ball AJ, Son L, Hanh NV, Tu ND, Lien NG, et al.: Multiplex PCR assay for malaria vector Anopheles minimus and four related species in the Myzomyia Series from Southeast Asia. Med Vet Entomol 2003, 17:423-8.
- [11]Marinotti O, Calvo E, Nguyen QK, Dissanayake S, Ribeiro JMC, James AA: Genome-wide analysis of gene expression in adult Anopheles gambiae. Insect Mol Biol 2006, 15:1-12.
- [12]Rinker DC, Pitts RJ, Zhou X, Suh E, Rokas A, Zwiebel LJ: Blood meal-induced changes to antennal transcriptome pro fi les reveal shifts in odor sensitivities in Anopheles gambiae. Proc Natl Acad Sci U S A 2013, 110:8260-5.
- [13]Pitts RJ, Rinker DC, Jones PL, Rokas A, Zwiebel LJ: Transcriptome profiling of chemosensory appendages in the malaria vector Anopheles gambiae reveals tissue- and sex-specific signatures of odor coding. BMC Genomics 2011, 12:271. BioMed Central Full Text
- [14]Crawford JE, Guelbeogo WM, Sanou A, Traoré A, Vernick KD, Sagnon N, et al.: De novo transcriptome sequencing in Anopheles funestus using Illumina RNA-seq technology. PLoS One 2010., 5Article ID e14202
- [15]Nie L, Wu H-J, Hsu J-M, Chang S-S, Labaff AM, Li C-W, et al.: Long non-coding RNAs: versatile master regulators of gene expression and crucial players in cancer. Am J Transl Res 2012, 4:127-50.
- [16]Kung JTY, Colognori D, Lee JT: Long noncoding RNAs: past, present, and future. Genetics 2013, 193:651-69.
- [17]Fatica A, Bozzoni I: Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 2014, 15:7-21.
- [18]Padrón A, Molina-Cruz A, Quinones M, Ribeiro JM, Ramphul U, Rodrigues J, et al.: In depth annotation of the Anopheles gambiae mosquito midgut transcriptome. BMC Genomics 2014, 15:636. BioMed Central Full Text
- [19]Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, et al.: Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 2009, 458:223-7.
- [20]Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, et al.: The transcriptional landscape of the mammalian genome. Science 2005, 309:1559-63.
- [21]Young RS, Marques AC, Tibbit C, Haerty W, Bassett AR, Liu J-L, et al.: Identification and properties of 1,119 candidate lincRNA loci in the Drosophila melanogaster genome. Genome Biol Evol 2012, 4:427-42.
- [22]Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP: Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 2011, 147:1537-50.
- [23]Nam J-W, Bartel DP: Long noncoding RNAs in C. elegans. Genome Res 2012, 22:2529-40.
- [24]Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, et al.: GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res 2012, 22:1760-74.
- [25]Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M: An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74.
- [26]Hangauer MJ, Vaughn IW, McManus MT: Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs. PLoS Genet 2013., 9Article ID e1003569
- [27]Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, et al.: Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res 2012, 22:577-91.
- [28]Soshnev A, Ishimoto H, McAllister BF, Li X, Wehling MD, Kitamoto T, et al.: A conserved long noncoding RNA affects sleep behavior in Drosophila. Genetics 2011, 189:455-68.
- [29]Li M, Wen S, Guo X, Bai B, Gong Z, Liu X, et al.: The novel long non-coding RNA CRG regulates Drosophila locomotor behavior. Nucleic Acids Res 2012, 40:11714-27.
- [30]Lv J, Liu H, Huang Z, Su J, He H, Xiu Y, et al.: Long non-coding RNA identification over mouse brain development by integrative modeling of chromatin and genomic features. Nucleic Acids Res 2013, 41:10044-61.
- [31]Heard E, Disteche CM: Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev 2006, 20:1848-67.
- [32]Mercer TR, Mattick JS: Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 2013, 20:300-7.
- [33]Necsulea A, Soumillon M, Warnefors M, Liechti A, Daish T, Zeller U, et al.: The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 2014, 505:635-40.
- [34]Kutter C, Watt S, Stefflova K, Wilson MD, Goncalves A, Ponting CP, et al.: Rapid turnover of long noncoding RNAs and the evolution of gene expression. PLoS Genet 2012., 8Article ID e1002841
- [35]Necsulea A, Kaessmann H: Evolutionary dynamics of coding and non-coding transcriptomes. Nat Rev Genet 2014, 15:734-48.
- [36]Wahlestedt C: Targeting long non-coding RNA to therapeutically upregulate gene expression. Nat Rev Drug Discov 2013, 12:433-46.
- [37]Lucas KJ, Myles KM, Raikhel AS: Small RNAs: a new frontier in mosquito biology. Trends Parasitol 2013, 29:295-303.
- [38]Burt A: Heritable strategies for controlling insect vectors of disease. Philos Trans R Soc Lond B Biol Sci 2014, 369:20130432.
- [39]Patro R, Mount SM, Kingsford C: Sailfish enables alignment-free isoform quantification from RNA-seq reads using lightweight algorithms. Nat Biotechnol 2014, 32:462-4.
- [40]Hu Z-L, Bao J, Reecy J: CateGOrizer: A Web-Based Program to Batch Analyze Gene Ontology Classification Categories. OJB 2008, 9:108-12.
- [41]Huang DW, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
- [42]Vogel H, Badapanda C, Knorr E, Vilcinskas A: RNA-sequencing analysis reveals abundant developmental stage-specific and immunity-related genes in the pollen beetle Meligethes aeneus. Insect Mol Biol 2014, 23:98-112.
- [43]Sun K, Chen X, Jiang P, Song X, Wang H, Sun H: iSeeRNA: identification of long intergenic non-coding RNA transcripts from transcriptome sequencing data. BMC Genomics 2013, 14(Suppl 2):S7.
- [44]Sun L, Zhang Z, Bailey TL, Perkins AC, Tallack MR, Xu Z, et al.: Prediction of novel long non-coding RNAs based on RNA-Seq data of mouse Klf1 knockout study. BMC Bioinformatics 2012, 13:331. BioMed Central Full Text
- [45]Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, et al.: The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 2012, 22:1775-89.
- [46]Wood EJ, Chin-Inmanu K, Jia H, Lipovich L: Sense-antisense gene pairs: sequence, transcription, and structure are not conserved between human and mouse. Front Genet 2013, 4(September):183.
- [47]Engström PG, Suzuki H, Ninomiya N, Akalin A, Sessa L, Lavorgna G, et al.: Complex Loci in human and mouse genomes. PLoS Genet 2006., 2Article ID e47
- [48]Novikova IV, Hennelly SP, Sanbonmatsu KY: Sizing up long non-coding RNAs: do lncRNAs have secondary and tertiary structure? Bioarchitecture 2012, 2:189-99.
- [49]Will S, Yu M, Berger B: Structure-based whole-genome realignment reveals many novel noncoding RNAs. Genome Res 2013, 23:1018-27.
- [50]Smith M a, Gesell T, Stadler PF, Mattick JS: Widespread purifying selection on RNA structure in mammals. Nucleic Acids Res 2013, 41:8220-36.
- [51]Wyder S, Kriventseva EV, Schröder R, Kadowaki T, Zdobnov EM: Quantification of ortholog losses in insects and vertebrates. Genome Biol 2007, 8:R242. BioMed Central Full Text
- [52]Richards S, Gibbs R a, Weinstock GM, Brown SJ, Denell R, Beeman RW, et al.: The genome of the model beetle and pest Tribolium castaneum. Nature 2008, 452:949-55.
- [53]Jensen TH, Jacquier A, Libri D: Dealing with pervasive transcription. Mol Cell 2013, 52:473-84.
- [54]Takken W, Knols BG: Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 1999, 44:131-57.
- [55]Paaijmans KP, Thomas MB: The influence of mosquito resting behaviour and associated microclimate for malaria risk. Malar J 2011, 10:183. BioMed Central Full Text
- [56]Lee JT: Epigenetic regulation by long noncoding RNAs. Science 2012, 338:1435-9.
- [57]Ponting CP, Oliver PL, Reik W: Evolution and functions of long noncoding RNAs. Cell 2009, 136:629-41.
- [58]Pates H, Curtis C: Mosquito behavior and vector control. Annu Rev Entomol 2005, 50:53-70.
- [59]RepeatMasker Open-3.0
- [60]Megy K, Emrich SJ, Lawson D, Campbell D, Dialynas E, Hughes DST, et al.: VectorBase: improvements to a bioinformatics resource for invertebrate vector genomics. Nucleic Acids Res 2012, 40(Database issue):D729-34.
- [61]Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL: TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013, 14:R36. BioMed Central Full Text
- [62]Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L: Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 2013, 31:46-53.
- [63]Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al.: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28:511-5.
- [64]Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, et al.: Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 2010, 28:503-10.
- [65]Lawniczak MKN, Emrich SJ, Holloway AK, Regier AP, Olson M, White B, et al.: Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 2010, 330(no. 6003):512-4.
- [66]Neafsey DE, Waterhouse RM, Abai MR, Aganezov SS, Max A, Allen JE, et al. Reports Highly evolvable malaria vectors : The genomes of 16 Anopheles mosquitoes. 2014(November):1–19.
- [67]Marinotti O, Cerqueira GC, de Almeida LGP, Ferro MIT, Loreto ELDS, Zaha A, et al.: The genome of Anopheles darlingi, the main neotropical malaria vector. Nucleic Acids Res 2013, 41:7387-400.
- [68]Jiang X, Peery A, Hall A, Sharma A, Chen X-G, Waterhouse RM, et al.: Genome analysis of a major urban malaria vector mosquito, Anopheles stephensi. Genome Biol 2014, 15:459. BioMed Central Full Text
- [69]Blanchette M, Kent WJ, Riemer C, Elnitski L, Smit AFA, Roskin KM, et al.: Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res 2004, 14:708-15.
- [70]Stark A, Lin MF, Kheradpour P, Pedersen JS, Parts L, Carlson JW, et al.: Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures. Nature 2007, 450:219-32.
- [71]Lindblad-Toh K, Garber M, Zuk O, Lin MF, Parker BJ, Washietl S, et al.: A high-resolution map of human evolutionary constraint using 29 mammals. Nature 2011, 478:476-82.
- [72]RepeatModeler Open-1.0
- [73]Stamatakis A: RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014, 30:1312-3.
- [74]Birney E, Clamp M, Durbin R: GeneWise and Genomewise. Genome Res 2004, 14:988-95.
- [75]Waterhouse RM, Tegenfeldt F, Li J, Zdobnov EM, Kriventseva EV: OrthoDB: a hierarchical catalog of animal, fungal and bacterial orthologs. Nucleic Acids Res 2013, 41(Database issue):D358-65.
- [76]Nene V, Wortman JR, Lawson D, Haas B, Kodira C, Tu ZJ, et al.: Genome sequence of Aedes aegypti, a major arbovirus vector. Science 2007, 316:1718-23.
- [77]Arensburger P, Megy K, Waterhouse RM, Abrudan J, Amedeo P, Antelo B, et al.: Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 2010, 330:86-8.
- [78]Lin MF, Jungreis I, Kellis M: PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics 2011, 27:i275-82.
- [79]Finn RD, Bateman A, Clements J, Coggill P, Eberhardt Y, Eddy SR, et al.: Pfam : the protein families database. Nucleic Acids Research 2014, 42:222-30.
- [80]Gough J, Karplus K, Hughey R, Chothia C: Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 2001, 313:903-19.
- [81]Haft DH, Selengut JD, White O: The TIGRFAMs database of protein families. Nucleic Acids Research 2003, 31:371-3.
- [82]Finn RD, Clements J, Eddy SR: HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011, 39(Web Server issue):W29-37.
- [83]Consortium TGO: Gene Ontology : tool for the unification of biology. Nature 2000, 25:25-9.
- [84]Hubisz MJ, Pollard KS, Siepel A: PHAST and RPHAST: phylogenetic analysis with space/time models. Brief Bioinform 2011, 12(no. 1):41-51.
- [85]Gruber A., Findeiß S, Washietl S, Hofacker I., Stadlet PF. RNAz 2.0: improved noncoding RNA detection. Pacific Symp Biocomput. 2010:69–79.
- [86]Thorvaldsdóttir H, Robinson JT, Mesirov JP: Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 2013, 14:178-92.
- [87]Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al.: Integrative genomics viewer. Nat Biotechnol 2011, 29:24-6.