MicroRNA-133 Inhibits Behavioral Aggregation by Controlling Dopamine Synthesis in Locusts

English version České info

Phenotypic plasticity is ubiquitous and primarily controlled by interactions between environmental and genetic factors. The migratory locust, a worldwide pest, exhibits pronounced phenotypic plasticity, which is a population density-dependent transition that occurs between the gregarious and solitary phases. Genes involved in dopamine synthesis have been shown to regulate the phase transition of locusts. However, the function of microRNAs in this process remains unknown. In this study, we report the participation of miR-133 in dopamine production and the behavioral transition by negatively regulating two critical genes, henna and pale, in the dopamine pathway. miR-133 participated in the post-transcriptional regulation of henna and pale by binding to their coding region and 3′ untranslated region, respectively. miR-133 displayed cellular co-localization with henna/pale in the protocerebrum, and its expression in the protocerebrum was negatively correlated with henna and pale expression. Moreover, miR-133 agomir delivery suppressed henna and pale expression, which consequently decreased dopamine production, thus resulting in the behavioral shift of the locusts from the gregarious phase to the solitary phase. Increasing the dopamine content could rescue the solitary phenotype, which was induced by miR-133 agomir delivery. Conversely, miR-133 inhibition increased the expression of henna and pale, resulting in the gregarious-like behavior of solitary locusts; this gregarious phenotype could be rescued by RNA interference of henna and pale. This study shows the novel function and modulation pattern of a miRNA in phenotypic plasticity and provides insight into the underlying molecular mechanisms of the phase transition of locusts.

Vyšlo v časopise: MicroRNA-133 Inhibits Behavioral Aggregation by Controlling Dopamine Synthesis in Locusts. PLoS Genet 10(2): e32767. doi:10.1371/journal.pgen.1004206
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004206

Souhrn

Zdroje

1. CaspiA, MoffittTE (2006) Gene-environment interactions in psychiatry: joining forces with neuroscience. Nat Rev Neurosci 7 : 583–590.

2. GretherGF (2005) Environmental change, phenotypic plasticity, and genetic compensation. Am Nat 166: E115–123.

3. NusseyDH, PostmaE, GienappP, VisserME (2005) Selection on heritable phenotypic plasticity in a wild bird population. Science 310 : 304–306.

4. KangL, ChenXY, ZhouY, LiuBW, ZhengW, et al. (2004) The analysis of large-scale gene expression correlated to the phase changes of the migratory locust. Proceedings of the National Academy of Sciences of the United States of America 101 : 17611–17615.

5. MaZY, YuJ, KangL (2006) LocustDB: a relational database for the transcriptome and biology of the migratory locust (Locusta migratoria). Bmc Genomics 7 : 11.

6. MaZY, GuoW, GuoXJ, WangXH, KangL (2011) Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway. Proceedings of the National Academy of Sciences of the United States of America 108 : 3882–3887.

7. GuoW, WangXH, MaZY, XueLA, HanJY, et al. (2011) CSP and Takeout Genes Modulate the Switch between Attraction and Repulsion during Behavioral Phase Change in the Migratory Locust. Plos Genetics 7 (2) e1001291.

8. WuR, WuZ, WangX, YangP, YuD, et al. (2012) Metabolomic analysis reveals that carnitines are key regulatory metabolites in phase transition of the locusts. Proc Natl Acad Sci U S A 109 : 3259–3263.

9. JiangF, YangM, GuoW, WangX, KangL (2012) Large-scale transcriptome analysis of retroelements in the migratory locust, Locusta migratoria. PLoS One 7: e40532.

10. RhoadesMW, ReinhartBJ, LimLP, BurgeCB, BartelB, et al. (2002) Prediction of plant microRNA targets. Cell 110 : 513–520.

11. AxtellMJ, WestholmJO, LaiEC (2011) Vive la difference: biogenesis and evolution of microRNAs in plants and animals. Genome Biology 12 (4) 221.

12. LaiEC (2003) microRNAs: Runts of the genome assert themselves. Current Biology 13: R925–R936.

13. FlyntAS, LaiEC (2008) Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nature Reviews Genetics 9 : 831–842.

14. DuursmaAM, KeddeM, SchrierM, le SageC, AgamiR (2008) miR-148 targets human DNMT3b protein coding region. RNA 14 : 872–877.

15. BartelDP (2004) MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116 : 281–297.

16. AmbrosV (2004) The functions of animal microRNAs. Nature 431 : 350–355.

17. PillaiRS (2005) MicroRNA function: Multiple mechanisms for a tiny RNA? Rna-a Publication of the Rna Society 11 : 1753–1761.

18. VasudevanS, TongY, SteitzJA (2007) Switching from repression to activation: microRNAs can up-regulate translation. Science 318 : 1931–1934.

19. LiX, CassidyJJ, ReinkeCA, FischboeckS, CarthewRW (2009) A microRNA imparts robustness against environmental fluctuation during development. Cell 137 : 273–282.

20. BiggarKK, DubucA, StoreyK (2009) MicroRNA regulation below zero: differential expression of miRNA-21 and miRNA-16 during freezing in wood frogs. Cryobiology 59 : 317–321.

21. BiggarKK, StoreyKB (2011) The emerging roles of microRNAs in the molecular responses of metabolic rate depression. J Mol Cell Biol 3 : 167–175.

22. BiggarKK, StoreyKB (2012) Evidence for cell cycle suppression and microRNA regulation of cyclin D1 during anoxia exposure in turtles. Cell Cycle 11 : 1705–1713.

23. MorinPJr, DubucA, StoreyKB (2008) Differential expression of microRNA species in organs of hibernating ground squirrels: a role in translational suppression during torpor. Biochim Biophys Acta 1779 : 628–633.

24. WeiYY, ChenS, YangPC, MaZY, KangL (2009) Characterization and comparative profiling of the small RNA transcriptomes in two phases of locust. Genome Biology 10 (1) R6.

25. RajewskyN (2006) microRNA target predictions in animals. Nat Genet 38 Suppl: S8–13.

26. Phillips-PortilloJ, StrausfeldNJ (2012) Representation of the brain's superior protocerebrum of the flesh fly, Neobellieria bullata, in the central body. J Comp Neurol 520 : 3070–3087.

27. MaZ, GuoW, GuoX, WangX, KangL (2011) Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway. Proc Natl Acad Sci U S A 108 : 3882–3887.

28. KimJ, InoueK, IshiiJ, VantiWB, VoronovSV, et al. (2007) A MicroRNA feedback circuit in midbrain dopamine neurons. Science 317 : 1220–1224.

29. YinVP, LepilinaA, SmithA, PossKD (2012) Regulation of zebrafish heart regeneration by miR-133. Dev Biol 365 : 319–327.

30. ShanH, ZhangY, LuY, ZhangY, PanZ, et al. (2009) Downregulation of miR-133 and miR-590 contributes to nicotine-induced atrial remodelling in canines. Cardiovasc Res 83 : 465–472.

31. PlasterkRH (2006) Micro RNAs in animal development. Cell 124 : 877–881.

32. KowarschA, MarrC, SchmidlD, RueppA, TheisFJ (2010) Tissue-specific target analysis of disease-associated microRNAs in human signaling pathways. PLoS One 5: e11154.

33. BaekD, VillenJ, ShinC, CamargoFD, GygiSP, et al. (2008) The impact of microRNAs on protein output. Nature 455 : 64–71.

34. InuiM, MartelloG, PiccoloS (2010) MicroRNA control of signal transduction. Nature Reviews Molecular Cell Biology 11 : 252–263.

35. HumphreysDT, WestmanBJ, MartinDI, PreissT (2005) MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. Proc Natl Acad Sci U S A 102 : 16961–16966.

36. PillaiRS, BhattacharyyaSN, ArtusCG, ZollerT, CougotN, et al. (2005) Inhibition of translational initiation by Let-7 microRNA in human cells. Science 309 : 1573–1576.

37. PetersenCP, BordeleauME, PelletierJ, SharpPA (2006) Short RNAs repress translation after initiation in mammalian cells. Mol Cell 21 : 533–542.

38. ChendrimadaTP, FinnKJ, JiX, BaillatD, GregoryRI, et al. (2007) MicroRNA silencing through RISC recruitment of eIF6. Nature 447 : 823–828.

39. OromUA, NielsenFC, LundAH (2008) MicroRNA-10a binds the 5′UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 30 : 460–471.

40. TayY, ZhangJ, ThomsonAM, LimB, RigoutsosI (2008) MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455 : 1124–1128.

41. GuoHL, IngoliaNT, WeissmanJS, BartelDP (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466 : 835–U866.

42. BazziniAA, LeeMT, GiraldezAJ (2012) Ribosome Profiling Shows That miR-430 Reduces Translation Before Causing mRNA Decay in Zebrafish. Science 336 : 233–237.

43. DjuranovicS, NahviA, GreenR (2012) miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336 : 237–240.

44. ZhangD, LiX, ChenC, LiY, ZhaoL, et al. (2012) Attenuation of p38-mediated miR-1/133 expression facilitates myoblast proliferation during the early stage of muscle regeneration. PLoS One 7: e41478.

45. ChenSA, YangPC, JiangF, WeiYY, MaZY, et al. (2010) De Novo Analysis of Transcriptome Dynamics in the Migratory Locust during the Development of Phase Traits. Plos One 5 (12) e15633.

46. WangXG, GuoBS, LiQ, PengJ, YangZJ, et al. (2013) miR-214 targets ATF4 to inhibit bone formation. Nature Medicine 19 : 93–100.

47. KrutzfeldtJ, RajewskyN, BraichR, RajeevKG, TuschlT, et al. (2005) Silencing of microRNAs in vivo with ‘antagomirs’. Nature 438 : 685–689.

48. NuovoGJ, EltonTS, Nana-SinkamP, VoliniaS, CroceCM, et al. (2009) A methodology for the combined in situ analyses of the precursor and mature forms of microRNAs and correlation with their putative targets. Nat Protoc 4 : 107–115.

49. NoldusLPJJ, SpinkAJ, TegelenboschRAJ (2001) EthoVision: a versatile video tracking system for automation of behavioral experiments. Behavior Research Methods 33 : 398–414.

50. RoessinghP, SimpsonSJ, JamesS (1993) Analysis of Phase-Related Changes in Behavior of Desert Locust Nymphs. Proceedings of the Royal Society of London Series B-Biological Sciences 252 : 43–49.

51. AnsteyML, RogersSM, OttSR, BurrowsM, SimpsonSJ (2009) Serotonin mediates behavioral gregarization underlying swarm formation in desert locusts. Science 323 : 627–630.