Dynamic miRNA-mRNA interactions coordinate gene expression in adult Anopheles gambiae
Autoři:
Xiaonan Fu aff001; Pengcheng Liu aff002; George Dimopoulos aff003; Jinsong Zhu aff002
Působiště autorů:
The Interdisciplinary Ph.D. Program in Genetics, Bioinformatics, and Computational Biology, Virginia Tech, Blacksburg, Virginia, United States of America
aff001; Department of Biochemistry, Virginia Tech, Blacksburg, Virginia, United States of America
aff002; W. Harry Feinstone Department of Molecular Microbiology and Immunology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland, United States of America
aff003
Vyšlo v časopise:
Dynamic miRNA-mRNA interactions coordinate gene expression in adult Anopheles gambiae. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008765
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008765
Souhrn
microRNAs (miRNAs) are increasingly recognized as important regulators of many biological processes in mosquitoes, vectors of numerous devastating infectious diseases. Identification of bona fide targets remains the bottleneck for functional studies of miRNAs. In this study, we used CLEAR-CLIP assays to systematically analyze miRNA-mRNA interactions in adult female Anopheles gambiae mosquitoes. Thousands of miRNA-target pairs were captured after direct ligation of the miRNA and its cognate target transcript in endogenous Argonaute–miRNA–mRNA complexes. Using two interactions detected in this manner, miR-309-SIX4 and let-7-kr-h1, we demonstrated the reliability of this experimental approach in identifying in vivo gene regulation by miRNAs. The miRNA-mRNA interaction dataset provided an invaluable opportunity to decipher targeting rules of mosquito miRNAs. Enriched motifs in the diverse targets of each miRNA indicated that the majority of mosquito miRNAs rely on seed-based canonical target recognition, while noncanonical miRNA binding sites are widespread and often contain motifs complementary to the central or 3’ ends of miRNAs. The time-lapse study of miRNA-target interactomes in adult female mosquitoes revealed dynamic miRNA regulation of gene expression in response to varying nutritional sources and physiological demands. Interestingly, some miRNAs exhibited flexibility to use distinct sequences at different stages for target recognition. Furthermore, many miRNA-mRNA interactions displayed stage-specific patterns, especially for those genes involved in metabolism, suggesting that miRNAs play critical roles in precise control of gene expression to cope with enormous physiological demands associated with egg production. The global mapping of miRNA-target interactions contributes to our understanding of miRNA targeting specificity in non-model organisms. It also provides a roadmap for additional studies focused on regulatory functions of miRNAs in Anopheles gambiae.
Klíčová slova:
Blood – Gene expression – Luciferase – Messenger RNA – MicroRNAs – Mosquitoes – RNA sequencing – Sequence motif analysis
Zdroje
1. Franklinos LHV, Jones KE, Redding DW, Abubakar I. The effect of global change on mosquito-borne disease. Lancet Infect Dis. 2019;19:e302–e12. Epub 2019/06/23. doi: 10.1016/S1473-3099(19)30161-6 31227327.
2. Hansen IA, Attardo GM, Rodriguez SD, Drake LL. Four-way regulation of mosquito yolk protein precursor genes by juvenile hormone-, ecdysone-, nutrient-, and insulin-like peptide signaling pathways. Front Physiol. 2014;5:103. doi: 10.3389/fphys.2014.00103 WOS:000346841400001. 24688471
3. Vanhandel E. Metabolism of Nutrients in the Adult Mosquito. Mosq News. 1984;44(4):573–9. WOS:A1984AAP4300025.
4. Telang A, Li Y, Noriega FG, Brown MR. Effects of larval nutrition on the endocrinology of mosquito egg development. The Journal of experimental biology. 2006;209(Pt 4):645–55. Epub 2006/02/02. doi: 10.1242/jeb.02026 16449559.
5. Thompson SN. Trehalose—The insect 'blood' sugar. Advances in Insect Physiology, Vol 31. 2003;31:205–85. doi: 10.1016/S0065-2806(03)31004-5 WOS:000187509900004.
6. Zou Z, Saha TT, Roy S, Shin SW, Backman TW, Girke T, et al. Juvenile hormone and its receptor, methoprene-tolerant, control the dynamics of mosquito gene expression. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(24):E2173–81. Epub 2013/05/02. doi: 10.1073/pnas.1305293110 23633570; PubMed Central PMCID: PMC3683779.
7. Jindra M, Palli SR, Riddiford LM. The juvenile hormone signaling pathway in insect development. Annual review of entomology. 2013;58:181–204. Epub 2012/09/22. doi: 10.1146/annurev-ento-120811-153700 22994547.
8. Athenstaedt K, Daum G. The life cycle of neutral lipids: synthesis, storage and degradation. Cell Mol Life Sci. 2006;63(12):1355–69. doi: 10.1007/s00018-006-6016-8 WOS:000238531600002. 16649142
9. Steele JE. Glycogen-Phosphorylase in Insects. Insect Biochem. 1982;12(2):131–47. doi: 10.1016/0020-1790(82)90001-4 WOS:A1982NN86300001.
10. Zhou GL, Pennington JE, Wells MA. Utilization of pre-existing energy stores of female Aedes aegypti mosquitoes during the first gonotrophic cycle. Insect biochemistry and molecular biology. 2004;34(9):919–25. doi: 10.1016/j.ibmb.2004.05.009 WOS:000224001200004. 15350611
11. Bonizzoni M, Dunn WA, Campbell CL, Olson KE, Dimon MT, Marinotti O, et al. RNA-seq analyses of blood-induced changes in gene expression in the mosquito vector species, Aedes aegypti. BMC genomics. 2011;12:82. Epub 2011/02/01. doi: 10.1186/1471-2164-12-82 21276245; PubMed Central PMCID: PMC3042412.
12. Hou Y, Wang XL, Saha TT, Roy S, Zhao B, Raikhel AS, et al. Temporal Coordination of Carbohydrate Metabolism during Mosquito Reproduction. PLoS genetics. 2015;11(7):e1005309. Epub 2015/07/15. doi: 10.1371/journal.pgen.1005309 26158648; PubMed Central PMCID: PMC4497655.
13. Wang X, Hou Y, Saha TT, Pei G, Raikhel AS, Zou Z. Hormone and receptor interplay in the regulation of mosquito lipid metabolism. Proceedings of the National Academy of Sciences of the United States of America. 2017;114(13):E2709–E18. Epub 2017/03/16. doi: 10.1073/pnas.1619326114 28292900; PubMed Central PMCID: PMC5380040.
14. Bryant B, Macdonald W, Raikhel AS. microRNA miR-275 is indispensable for blood digestion and egg development in the mosquito Aedes aegypti. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(52):22391–8. Epub 2010/12/01. doi: 10.1073/pnas.1016230107 21115818; PubMed Central PMCID: PMC3012520.
15. Ling L, Kokoza VA, Zhang C, Aksoy E, Raikhel AS. MicroRNA-277 targets insulin-like peptides 7 and 8 to control lipid metabolism and reproduction in Aedes aegypti mosquitoes. Proceedings of the National Academy of Sciences of the United States of America. 2017;114(38):E8017–E24. Epub 2017/09/07. doi: 10.1073/pnas.1710970114 28874536; PubMed Central PMCID: PMC5617303.
16. Liu S, Lucas KJ, Roy S, Ha J, Raikhel AS. Mosquito-specific microRNA-1174 targets serine hydroxymethyltransferase to control key functions in the gut. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(40):14460–5. Epub 2014/09/24. doi: 10.1073/pnas.1416278111 25246546; PubMed Central PMCID: PMC4209991.
17. Lucas KJ, Roy S, Ha J, Gervaise AL, Kokoza VA, Raikhel AS. MicroRNA-8 targets the Wingless signaling pathway in the female mosquito fat body to regulate reproductive processes. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(5):1440–5. Epub 2015/01/22. doi: 10.1073/pnas.1424408112 25605933; PubMed Central PMCID: PMC4321257.
18. Zhang Y, Zhao B, Roy S, Saha TT, Kokoza VA, Li M, et al. microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti. Proceedings of the National Academy of Sciences of the United States of America. 2016;113(33):E4828–36. Epub 2016/08/05. doi: 10.1073/pnas.1609792113 27489347; PubMed Central PMCID: PMC4995966.
19. Zhao B, Lucas KJ, Saha TT, Ha J, Ling L, Kokoza VA, et al. MicroRNA-275 targets sarco/endoplasmic reticulum Ca2+ adenosine triphosphatase (SERCA) to control key functions in the mosquito gut. PLoS genetics. 2017;13(8):e1006943. Epub 2017/08/09. doi: 10.1371/journal.pgen.1006943 28787446; PubMed Central PMCID: PMC5560755.
20. Bushati N, Cohen SM. microRNA functions. Annual review of cell and developmental biology. 2007;23:175–205. Epub 2007/05/18. doi: 10.1146/annurev.cellbio.23.090506.123406 17506695.
21. Hausser J, Zavolan M. Identification and consequences of miRNA-target interactions—beyond repression of gene expression. Nature reviews Genetics. 2014;15(9):599–612. Epub 2014/07/16. doi: 10.1038/nrg3765 25022902.
22. Didiano D, Hobert O. Molecular architecture of a miRNA-regulated 3' UTR. Rna. 2008;14(7):1297–317. doi: 10.1261/rna.1082708 18463285; PubMed Central PMCID: PMC2441980.
23. Gu S, Jin L, Zhang F, Sarnow P, Kay MA. Biological basis for restriction of microRNA targets to the 3' untranslated region in mammalian mRNAs. Nature structural & molecular biology. 2009;16(2):144–50. doi: 10.1038/nsmb.1552 19182800; PubMed Central PMCID: PMC2713750.
24. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell. 2006;125(6):1111–24. doi: 10.1016/j.cell.2006.04.031 16777601.
25. Kedde M, Strasser MJ, Boldajipour B, Oude Vrielink JA, Slanchev K, le Sage C, et al. RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell. 2007;131(7):1273–86. doi: 10.1016/j.cell.2007.11.034 18155131.
26. Hammell CM, Lubin I, Boag PR, Blackwell TK, Ambros V. nhl-2 Modulates microRNA activity in Caenorhabditis elegans. Cell. 2009;136(5):926–38. doi: 10.1016/j.cell.2009.01.053 19269369; PubMed Central PMCID: PMC2670343.
27. Johnston M, Hutvagner G. Posttranslational modification of Argonautes and their role in small RNA-mediated gene regulation. Silence. 2011;2:5. doi: 10.1186/1758-907X-2-5 21943311; PubMed Central PMCID: PMC3199228.
28. Neumuller RA, Betschinger J, Fischer A, Bushati N, Poernbacher I, Mechtler K, et al. Mei-P26 regulates microRNAs and cell growth in the Drosophila ovarian stem cell lineage. Nature. 2008;454(7201):241–5. doi: 10.1038/nature07014 18528333; PubMed Central PMCID: PMC2988194.
29. Rudel S, Wang Y, Lenobel R, Korner R, Hsiao HH, Urlaub H, et al. Phosphorylation of human Argonaute proteins affects small RNA binding. Nucleic acids research. 2011;39(6):2330–43. doi: 10.1093/nar/gkq1032 21071408; PubMed Central PMCID: PMC3064767.
30. Mittal N, Zavolan M. Seq and CLIP through the miRNA world. Genome biology. 2014;15(1):202. Epub 2014/01/28. doi: 10.1186/gb4151 24460822; PubMed Central PMCID: PMC4053862.
31. Chi SW, Zang JB, Mele A, Darnell RB. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature. 2009;460(7254):479–86. Epub 2009/06/19. doi: 10.1038/nature08170 19536157; PubMed Central PMCID: PMC2733940.
32. Zisoulis DG, Lovci MT, Wilbert ML, Hutt KR, Liang TY, Pasquinelli AE, et al. Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nature structural & molecular biology. 2010;17(2):173–9. Epub 2010/01/12. doi: 10.1038/nsmb.1745 20062054; PubMed Central PMCID: PMC2834287.
33. Zhang X, Aksoy E, Girke T, Raikhel AS, Karginov FV. Transcriptome-wide microRNA and target dynamics in the fat body during the gonadotrophic cycle of Aedes aegypti. Proceedings of the National Academy of Sciences of the United States of America. 2017;114(10):E1895–E903. Epub 2017/02/23. doi: 10.1073/pnas.1701474114 28223504; PubMed Central PMCID: PMC5347622.
34. Moore MJ, Scheel TK, Luna JM, Park CY, Fak JJ, Nishiuchi E, et al. miRNA-target chimeras reveal miRNA 3'-end pairing as a major determinant of Argonaute target specificity. Nature communications. 2015;6:8864. Epub 2015/11/26. doi: 10.1038/ncomms9864 26602609; PubMed Central PMCID: PMC4674787.
35. Grosswendt S, Filipchyk A, Manzano M, Klironomos F, Schilling M, Herzog M, et al. Unambiguous identification of miRNA:target site interactions by different types of ligation reactions. Molecular cell. 2014;54(6):1042–54. Epub 2014/05/27. doi: 10.1016/j.molcel.2014.03.049 24857550; PubMed Central PMCID: PMC4181535.
36. Helwak A, Kudla G, Dudnakova T, Tollervey D. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell. 2013;153(3):654–65. Epub 2013/04/30. doi: 10.1016/j.cell.2013.03.043 23622248; PubMed Central PMCID: PMC3650559.
37. Biryukova I, Ye T, Levashina E. Transcriptome-wide analysis of microRNA expression in the malaria mosquito Anopheles gambiae. BMC genomics. 2014;15:557. Epub 2014/07/07. doi: 10.1186/1471-2164-15-557 24997592; PubMed Central PMCID: PMC4112208.
38. Fu X, Dimopoulos G, Zhu J. Association of microRNAs with Argonaute proteins in the malaria mosquito Anopheles gambiae after blood ingestion. Scientific reports. 2017;7(1):6493. Epub 2017/07/28. doi: 10.1038/s41598-017-07013-1 28747726.
39. Ojani R, Fu X, Ahmed T, Liu P, Zhu J. Kruppel homologue 1 acts as a repressor and an activator in the transcriptional response to juvenile hormone in adult mosquitoes. Insect molecular biology. 2018;27(2):268–78. Epub 2018/01/10. doi: 10.1111/imb.12370 29314423; PubMed Central PMCID: PMC5837916.
40. Song J, Li W, Zhao H, Gao L, Fan Y, Zhou S. The microRNAs let-7 and miR-278 regulate insect metamorphosis and oogenesis by targeting the juvenile hormone early-response gene Kruppel-homolog 1. Development. 2018;145(24). Epub 2018/11/25. doi: 10.1242/dev.170670 30470705.
41. Zhou G, Flowers M, Friedrich K, Horton J, Pennington J, Wells MA. Metabolic fate of [14C]-labeled meal protein amino acids in Aedes aegypti mosquitoes. Journal of insect physiology. 2004;50(4):337–49. Epub 2004/04/15. doi: 10.1016/j.jinsphys.2004.02.003 15081827.
42. Gebert LFR, MacRae IJ. Regulation of microRNA function in animals. Nat Rev Mol Cell Biol. 2019;20(1):21–37. Epub 2018/08/16. doi: 10.1038/s41580-018-0045-7 30108335; PubMed Central PMCID: PMC6546304.
43. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Molecular cell. 2007;27(1):91–105. Epub 2007/07/07. doi: 10.1016/j.molcel.2007.06.017 17612493; PubMed Central PMCID: PMC3800283.
44. Yu J, Ryan DG, Getsios S, Oliveira-Fernandes M, Fatima A, Lavker RM. MicroRNA-184 antagonizes microRNA-205 to maintain SHIP2 levels in epithelia. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(49):19300–5. Epub 2008/11/27. doi: 10.1073/pnas.0803992105 19033458; PubMed Central PMCID: PMC2587229.
45. Golden RJ, Chen B, Li T, Braun J, Manjunath H, Chen X, et al. An Argonaute phosphorylation cycle promotes microRNA-mediated silencing. Nature. 2017;542(7640):197–202. Epub 2017/01/24. doi: 10.1038/nature21025 28114302; PubMed Central PMCID: PMC5302127.
46. Ahuja D, Goyal A, Ray PS. Interplay between RNA-binding protein HuR and microRNA-125b regulates p53 mRNA translation in response to genotoxic stress. RNA biology. 2016;13(11):1152–65. Epub 2016/10/30. doi: 10.1080/15476286.2016.1229734 27592685; PubMed Central PMCID: PMC5100343.
47. Kedde M, van Kouwenhove M, Zwart W, Oude Vrielink JA, Elkon R, Agami R. A Pumilio-induced RNA structure switch in p27-3' UTR controls miR-221 and miR-222 accessibility. Nat Cell Biol. 2010;12(10):1014–20. Epub 2010/09/08. doi: 10.1038/ncb2105 20818387.
48. Lampe L, Levashina EA. MicroRNA Tissue Atlas of the Malaria Mosquito Anopheles gambiae. G3. 2018;8(1):185–93. Epub 2017/11/18. doi: 10.1534/g3.117.300170 29146584; PubMed Central PMCID: PMC5765347.
49. Jin H, Kim VN, Hyun S. Conserved microRNA miR-8 controls body size in response to steroid signaling in Drosophila. Genes & development. 2012;26(13):1427–32. Epub 2012/07/04. doi: 10.1101/gad.192872.112 22751499; PubMed Central PMCID: PMC3403011.
50. Wen J, Mohammed J, Bortolamiol-Becet D, Tsai H, Robine N, Westholm JO, et al. Diversity of miRNAs, siRNAs, and piRNAs across 25 Drosophila cell lines. Genome research. 2014;24(7):1236–50. Epub 2014/07/06. doi: 10.1101/gr.161554.113 24985917; PubMed Central PMCID: PMC4079977.
51. Roy S, Saha TT, Johnson L, Zhao B, Ha J, White KP, et al. Regulation of Gene Expression Patterns in Mosquito Reproduction. PLoS genetics. 2015;11(8):e1005450. Epub 2015/08/15. doi: 10.1371/journal.pgen.1005450 26274815; PubMed Central PMCID: PMC4537244.
52. Marinotti O, Calvo E, Nguyen QK, Dissanayake S, Ribeiro JM, James AA. Genome-wide analysis of gene expression in adult Anopheles gambiae. Insect molecular biology. 2006;15(1):1–12. Epub 2006/02/14. doi: 10.1111/j.1365-2583.2006.00610.x 16469063.
53. Mead EA, Li M, Tu Z, Zhu J. Translational regulation of Anopheles gambiae mRNAs in the midgut during Plasmodium falciparum infection. BMC genomics. 2012;13:366. Epub 2012/08/04. doi: 10.1186/1471-2164-13-366 22857387; PubMed Central PMCID: PMC3443010.
54. Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J, et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome biology. 2008;9(1):R7. Epub 2008/01/15. doi: 10.1186/gb-2008-9-1-r7 18190707; PubMed Central PMCID: PMC2395244.
55. Dodt M, Roehr JT, Ahmed R, Dieterich C. FLEXBAR-Flexible Barcode and Adapter Processing for Next-Generation Sequencing Platforms. Biology. 2012;1(3):895–905. Epub 2012/01/01. doi: 10.3390/biology1030895 24832523; PubMed Central PMCID: PMC4009805.
56. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. Journal of molecular biology. 1990;215(3):403–10. Epub 1990/10/05. doi: 10.1016/S0022-2836(05)80360-2 2231712.
57. Haecker I, Gay LA, Yang Y, Hu J, Morse AM, McIntyre LM, et al. Ago HITS-CLIP expands understanding of Kaposi's sarcoma-associated herpesvirus miRNA function in primary effusion lymphomas. PLoS pathogens. 2012;8(8):e1002884. Epub 2012/08/29. doi: 10.1371/journal.ppat.1002884 22927820; PubMed Central PMCID: PMC3426530.
58. Kruger J, Rehmsmeier M. RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic acids research. 2006;34(Web Server issue):W451–4. Epub 2006/07/18. doi: 10.1093/nar/gkl243 16845047; PubMed Central PMCID: PMC1538877.
59. Ojani R, Liu P, Fu X, Zhu J. Protein kinase C modulates transcriptional activation by the juvenile hormone receptor methoprene-tolerant. Insect biochemistry and molecular biology. 2016;70:44–52. Epub 2015/12/23. doi: 10.1016/j.ibmb.2015.12.001 26689644; PubMed Central PMCID: PMC4767628.
60. Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015;31(2):166–9. Epub 2014/09/28. doi: 10.1093/bioinformatics/btu638 25260700; PubMed Central PMCID: PMC4287950.
61. Zhong Y, Karaletsos T, Drewe P, Sreedharan VT, Kuo D, Singh K, et al. RiboDiff: detecting changes of mRNA translation efficiency from ribosome footprints. Bioinformatics. 2017;33(1):139–41. Epub 2016/09/17. doi: 10.1093/bioinformatics/btw585 27634950; PubMed Central PMCID: PMC5198522.
62. Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics. 2011;27(7):1017–8. Epub 2011/02/19. doi: 10.1093/bioinformatics/btr064 21330290; PubMed Central PMCID: PMC3065696.
63. Hafner A, Stewart-Ornstein J, Purvis JE, Forrester WC, Bulyk ML, Lahav G. p53 pulses lead to distinct patterns of gene expression albeit similar DNA-binding dynamics. Nature structural & molecular biology. 2017;24(10):840–7. Epub 2017/08/22. doi: 10.1038/nsmb.3452 28825732; PubMed Central PMCID: PMC5629117.
64. Eichler GS, Huang S, Ingber DE. Gene Expression Dynamics Inspector (GEDI): for integrative analysis of expression profiles. Bioinformatics. 2003;19(17):2321–2. Epub 2003/11/25. doi: 10.1093/bioinformatics/btg307 14630665.
65. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols. 2009;4(1):44–57. Epub 2009/01/10. doi: 10.1038/nprot.2008.211 19131956.
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