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Long noncoding RNA PAHAL modulates locust behavioural plasticity through the feedback regulation of dopamine biosynthesis


Autoři: Xia Zhang aff001;  Ya'nan Xu aff001;  Bing Chen aff001;  Le Kang aff001
Působiště autorů: State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China aff001;  Beijing Institute of Life Sciences, Chinese Academy of Sciences, Beijing, China aff002;  CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China aff003;  College of Life Sciences, Hebei University, Baoding, China aff004
Vyšlo v časopise: Long noncoding RNA PAHAL modulates locust behavioural plasticity through the feedback regulation of dopamine biosynthesis. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008771
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008771

Souhrn

Some long noncoding RNAs (lncRNAs) are specifically expressed in brain cells, implying their neural and behavioural functions. However, how lncRNAs contribute to neural regulatory networks governing the precise behaviour of animals is less explored. Here, we report the regulatory mechanism of the nuclear-enriched lncRNA PAHAL for dopamine biosynthesis and behavioural adjustment in migratory locusts (Locusta migratoria), a species with extreme behavioral plasticity. PAHAL is transcribed from the sense (coding) strand of the gene encoding phenylalanine hydroxylase (PAH), which is responsible for the synthesis of dopamine from phenylalanine. PAHAL positively regulates PAH expression resulting in dopamine production in the brain. In addition, PAHAL modulates locust behavioral aggregation in a population density-dependent manner. Mechanistically, PAHAL mediates PAH transcriptional activation by recruiting serine/arginine-rich splicing factor 2 (SRSF2), a transcription/splicing factor, to the PAH proximal promoter. The co-activation effect of PAHAL requires the interaction of the PAHAL/SRSF2 complex with the promoter-associated nascent RNA of PAH. Thus, the data support a model of feedback modulation of animal behavioural plasticity by an lncRNA. In this model, the lncRNA mediates neurotransmitter metabolism through orchestrating a local transcriptional loop.

Klíčová slova:

DNA transcription – Gene expression – Locusts – Long non-coding RNAs – Metabolic pathways – Nymphs – Small interfering RNAs – Transcriptional control


Zdroje

1. Mercer TR, Dinger ME, Mattick JS. Long non-coding RNAs: insights into functions. Nat Rev Genet. 2009; 10: 155–159. doi: 10.1038/nrg2521 19188922

2. Geisler S, Coller J. RNA in unexpected places: long non-coding RNA functions in diverse cellular contexts. Nat Rev Mol Cell Biol. 2013; 14: 699–712. doi: 10.1038/nrm3679 24105322

3. Quinn JJ, Chang HY. Unique features of long non-coding RNA biogenesis and function. Nat Rev Genet. 2016; 17: 47–62. doi: 10.1038/nrg.2015.10 26666209

4. Lee JT. The X as Model for RNA’s Niche in Epigenomic Regulation. Cold Spring Harbor Perspect Biol. 2010; 2: a003749. doi: 10.1101/cshperspect.a003749 20739414

5. Meller VH, Joshi SS, Deshpande N. Modulation of chromatin by noncoding RNA. Annu Rev Genet. 2015; 49: 673–695. doi: 10.1146/annurev-genet-112414-055205 26631517

6. Ohhata T, Senner CE, Hemberger M, Wutz A. Lineage-specific function of the noncoding Tsix RNA for Xist repression and Xi reactivation in mice. Gene Dev. 2011; 25: 1702–1715. doi: 10.1101/gad.16997911 21852535

7. Michelini F, Pitchiaya S, Vitelli V, Sharma S, Gioia U, Pessina F, et al. Damage-induced lncRNAs control the DNA damage response through interaction with DDRNAs at individual double-strand breaks. Nat Cell Biol. 2017; 19: 1400–1411. doi: 10.1038/ncb3643 29180822

8. Williamson L, Saponaro M, Boeing S, East P, Mitter R, Kantidakis T, et al. UV irradiation induces a non-coding RNA that functionally opposes the protein encoded by the same gene. Cell. 2017; 168: 1–13. doi: 10.1016/j.cell.2016.12.043

9. Fatica A, Bozzoni I. Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet. 2014; 15: 7–21. doi: 10.1038/nrg3606 24296535

10. Bian S, Sun T. Functions of noncoding RNAs in neural development and neurological diseases. Mol Neurobiol. 2011; 44: 359–373. doi: 10.1007/s12035-011-8211-3 21969146

11. Sallam T, Jones MC, Gilliland T, Zhang L, Wu X, Eskin A, et al. Feedback modulation of cholesterol metabolism by the lipid-responsive non-coding RNA LeXis. Nature. 2016; 534: 124–128. doi: 10.1038/nature17674 27251289

12. Liu X, Xiao Z-D, Han L, Zhang J, Lee S-W, Wang W, et al. LncRNA NBR2 engages a metabolic checkpoint by regulating AMPK under energy stress. Nat Cell Biol. 2016; 18: 431–442. doi: 10.1038/ncb3328 26999735

13. Tang YJ, Zhou T, Yu X, Xue ZX, Shen N. The role of long non-coding RNAs in rheumatic diseases. Nat Rev Rheumatol. 2017; 13: 657–669. doi: 10.1038/nrrheum.2017.162 28978995

14. Soreq L, Guffanti A, Salomonis N, Simchovitz A, Israel Z, Bergman H, et al. Long non-coding RNA and alternative splicing modulations in Parkinson's leukocytes identified by RNA sequencing. PLoS Comput Biol. 2014; 10: e1003517. doi: 10.1371/journal.pcbi.1003517 24651478

15. Qureshi IA, Mehler MF. Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease. Nat Rev Neurosci. 2012; 13: 528–541. doi: 10.1038/nrn3234 22814587

16. Peschansky VJ, Pastori C, Zeier Z, Wentzel K, Velmeshev D, Magistri M, et al. The long non-coding RNA FMR4 promotes proliferation of human neural precursor cells and epigenetic regulation of gene expression in trans. Mol Cell Neurosci. 2016; 74: 49–57. doi: 10.1016/j.mcn.2016.03.008 27001315

17. Schaukowitch K, Kim TK. Emerging epigenetic mechanisms of long non-coding RNAs. Neuroscience. 2014; 264: 25–38. doi: 10.1016/j.neuroscience.2013.12.009 24342564

18. Earls LR, Westmoreland JJ, Zakharenko SS. Non-coding RNA regulation of synaptic plasticity and memory: Implications for aging. Ageing Res Rev. 2014; 17: 34–42. doi: 10.1016/j.arr.2014.03.004 24681292

19. Rani N, Nowakowski TJ, Zhou H, Godshalk SE, Lisi V, Kriegstein AR, et al. A primate lncRNA mediates Notch signaling during neuronal development by sequestering miRNA. Neuron. 2016; 90: 1174–1188. doi: 10.1016/j.neuron.2016.05.005 27263970

20. Shields EJ, Sheng L, Weiner AK, Garcia BA, Bonasio R. High-quality genome assemblies reveal long non-coding RNAs expressed in Ant brains. Cell Rep. 2018; 23: 3078–3090. doi: 10.1016/j.celrep.2018.05.014 29874592

21. Sauvageau M, Goff LA, Lodato S, Bonev B, Groff AF, Gerhardinger C, et al. Multiple knockout mouse models reveal lincRNAs are required for life and brain development. Elife. 2013; 2: e01749. doi: 10.7554/eLife.01749 24381249

22. Soshnev AA, 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: 455–468. doi: 10.1534/genetics.111.131706 21775470

23. 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: 11714–11727. doi: 10.1093/nar/gks943 23074190

24. Engreitz JM, Haines JE, Perez EM, Munson G, Chen J, Kane M, et al. Local regulation of gene expression by lncRNA promoters, transcription and splicing. Nature. 2016; 539: 452–455. doi: 10.1038/nature20149 27783602

25. Guil S, Esteller M. Cis-acting noncoding RNAs: friends and foes. Nat Struct Mol Biol. 2012; 19: 1068–1075. doi: 10.1038/nsmb.2428 23132386

26. Marchese FP, Raimondi I, Huarte M. The multidimensional mechanisms of long noncoding RNA function. Genome Biol. 2017; 18: 206. doi: 10.1186/s13059-017-1348-2 29084573

27. Chen LL. Linking long noncoding RNA localization and function. Trends Biochem Sci. 2016; 41: 761–772. doi: 10.1016/j.tibs.2016.07.003 27499234

28. Csorba T, Questa JI, Sun Q, Dean C. Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization. Proc Natl Acad Sci USA. 2014; 111: 16160–16165. doi: 10.1073/pnas.1419030111 25349421

29. Raveendra BL, Swarnkar S, Avchalumov Y, Liu X-A, Grinman E, Badal K, et al. Long noncoding RNA GM12371 acts as a transcriptional regulator of synapse function. Proc Natl Acad Sci USA 2018; 115: E10197–E205. doi: 10.1073/pnas.1722587115 30297415

30. Spadaro PA, Flavell CR, Widagdo J, Ratnu VS, Troup M, Ragan C, et al. Long noncoding RNA-directed epigenetic regulation of gene expression is associated with anxiety-like behavior in mice. Biol Psychiat. 2015; 78: 848–859. doi: 10.1016/j.biopsych.2015.02.004 25792222

31. Ng SY, Lin L, Soh BS, Stanton LW. Long noncoding RNAs in development and disease of the central nervous system. Trends Genet. 2013; 29: 461–468. doi: 10.1016/j.tig.2013.03.002 23562612

32. Gepshtein S, Li XY, Snider J, Plank M, Lee D, Poizner H. Dopamine function and the efficiency of human movement. J Cognitive Neurosci. 2014; 26: 645–657. doi: 10.1162/jocn_a_00503 24144250

33. Cerovic M, d'Isa R, Tonini R, Brambilla R. Molecular and cellular mechanisms of dopamine-mediated behavioral plasticity in the striatum. Neurobiol Learn Mem. 2013; 105: 63–80. doi: 10.1016/j.nlm.2013.06.013 23827407

34. Coleman CM, Neckameyer WS. Substrate regulation of serotonin and dopamine synthesis in Drosophila. Invert Neurosci. 2004; 5: 85–96. doi: 10.1007/s10158-004-0031-y 15480914

35. Daubner SC, Le T, Wang S. Tyrosine hydroxylase and regulation of dopamine synthesis. Arch Biochem Biophys. 2011; 508: 1–12. doi: 10.1016/j.abb.2010.12.017 21176768

36. Yang M, Wei Y, Jiang F, Wang Y, Guo X, He J, et al. MicroRNA-133 inhibits behavioral aggregation by controlling dopamine synthesis in locusts. PLoS Genet. 2014; 10: e1004206. doi: 10.1371/journal.pgen.1004206 24586212

37. Ruiz-Vazquez P, Silva FJ. Aberrant splicing of the Drosophila melanogaster phenylalanine hydroxylase pre-mRNA caused by the insertion of a B104/roo transposable element in the Henna locus. Insect Biochem Mol Biol. 1999; 29: 311–318. doi: 10.1016/s0965-1748(99)00002-8 10333570

38. Wang X, Kang L. Molecular mechanisms of phase change in locusts. Annu Rev Entomol. 2014; 59: 225–244. doi: 10.1146/annurev-ento-011613-162019 24160426

39. Guo X, Ma Z, Kang L. Two dopamine receptors play different roles in phase change of the migratory locust. Front Behav Neurosci. 2015; 9: 80. doi: 10.3389/fnbeh.2015.00080 25873872

40. Ma Z, Guo W, Guo X, Wang X, Kang L. Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway. Proc Natl Acad Sci USA. 2011; 108: 3882–3887. doi: 10.1073/pnas.1015098108 21325054

41. Pener MP, Simpson SJ. Locust phase polyphenism: an update. Adv Insect Physiol. 2009; 36: 1–272. https://doi.org/10.1016/S0065-2806(08)36001-9

42. Guo W, Wang X, Ma Z, Xue L, Han J, Yu D, et al. CSP and takeout genes modulate the switch between attraction and repulsion during behavioral phase change in the migratory locust. PLoS Genet. 2011; 7: e1001291. doi: 10.1371/journal.pgen.1001291 21304893

43. Burrows M, Rogers SM, Ott SR. Epigenetic remodelling of brain, body and behaviour during phase change in locusts. Neural Syst Circuits. 2011; 1: 11. doi: 10.1186/2042-1001-1-11 22330837

44. Wang L, Park HJ, Dasari S, Wang S, Kocher JP, Li W. CPAT: Coding-potential assessment tool using an alignment-free logistic regression model. Nucleic Acids Res. 2013; 41: e74. doi: 10.1093/nar/gkt006 23335781

45. Coleman CM, Neckameyer WS. Serotonin synthesis by two distinct enzymes in Drosophila melanogaster. Arch Insect Biochem Physiol. 2005; 59: 12–31. doi: 10.1002/arch.20050 15822093

46. Neckameyer WS, White K. A single locus encodes both phenylalanine hydroxylase and tryptophan hydroxylase activities in Drosophila. J Biol Chem. 1992; 267: 4199–4206 1371286

47. Zhang B, Gunawardane L, Niazi F, Jahanbani F, Chen X, Valadkhan S. A novel RNA motif mediates the strict nuclear localization of a long noncoding RNA. Mol Cell Biol. 2014; 34: 2318–2329. doi: 10.1128/MCB.01673-13 24732794

48. Lin SR, Xiao R, Sun PQ, Xu XD, Fu XD. Dephosphorylation-dependent sorting of SR splicing factors during mRNP maturation. Mol Cell. 2005; 20: 413–425. doi: 10.1016/j.molcel.2005.09.015 16285923

49. Ji X, Zhou Y, Pandit S, Huang J, Li H, Lin CY, et al. SR proteins collaborate with 7SK and promoter-associated nascent RNA to release paused polymerase. Cell. 2013; 153: 855–868. doi: 10.1016/j.cell.2013.04.028 23663783

50. Homberg U. Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. J Comp Neurol. 1991; 303: 245–254. doi: 10.1002/cne.903030207 2013639

51. Wendt B, Homberg U. Immunocytochemistry of dopamine in the brain of the locust Schistocerca gregaria. J Comp Neurol. 1992; 321: 387–403. doi: 10.1002/cne.903210307 1506476

52. Homberg U. Neurotransmitters and neuropeptides in the brain of the locust. J Comp Neurol. 2002; 56: 189–209. doi: 10.1002/jemt.10024 11810722

53. Gil N, Ulitsky I. Regulation of gene expression by cis-acting long non-coding RNAs. Nat Rev Genet. 2020; 21: 102–117. doi: 10.1038/s41576-019-0184-5 31729473

54. Yan P, Luo S, Lu JY, Shen X. Cis- and trans-acting lncRNAs in pluripotency and reprogramming. Curr Opin Genet Dev. 2017; 46: 170–178. doi: 10.1016/j.gde.2017.07.009 28843809

55. Heo JB, Sung S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science. 2011; 331: 76–79. doi: 10.1126/science.1197349 21127216

56. Sun TT, He J, Liang Q, Ren LL, Yan TT, Yu TC, et al. Lncrna GClnc1 promotes gastric carcinogenesis and may act as a modular scaffold of WDR5 and KAT2A complexes to specify the histone modification pattern. Cancer Discov. 2016; 6: 784–801. doi: 10.1158/2159-8290.CD-15-0921 27147598

57. Chen B, Zhang Y, Zhang X, Jia S, Chen S, Kang L. Genome-wide identification and developmental expression profiling of long noncoding RNAs during Drosophila metamorphosis. Sci Rep. 2016; 6: 23330. doi: 10.1038/srep23330 26996731

58. Sarropoulos I, Marin R, Cardoso-Moreira M, Kaessmann H. Developmental dynamics of lncRNAs across mammalian organs and species. Nature. 2019, 571: 510–514. doi: 10.1038/s41586-019-1341-x 31243368

59. Sun Q, Hao Q, Prasanth KV. Nuclear long noncoding RNAs: key regulators of gene expression. Trends Genet. 2018, 34: 142–157. doi: 10.1016/j.tig.2017.11.005 29249332

60. Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature. 2011; 472: 120–124. doi: 10.1038/nature09819 21423168

61. Lin S, Fu XD. SR proteins and related factors in alternative splicing. Adv Exp Med Biol. 2007; 623: 107–122. doi: 10.1007/978-0-387-77374-2_7 18380343

62. Lin SR, Coutinho-Mansfield G, Wang D, Pandit S, Fu XD. The splicing factor SC35 has an active role in transcriptional elongation. Nat Struct Mol Biol. 2008; 15: 819–826. doi: 10.1038/nsmb.1461 18641664

63. Long JC, Caceres JF. The SR protein family of splicing factors: master regulators of gene expression. Biochem J. 2009; 417: 15–27. doi: 10.1042/BJ20081501 19061484

64. Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, et al. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell. 2010; 39: 925–938. doi: 10.1016/j.molcel.2010.08.011 20797886

65. Sapra AK, Anko ML, Grishina I, Lorenz M, Pabis M, Poser I, et al. SR protein family members display diverse activities in the formation of nascent and mature mRNPs in vivo. Mol Cell. 2009; 34: 179–190. doi: 10.1016/j.molcel.2009.02.031 19394295

66. Bernard D, Prasanth KV, Tripathi V, Colasse S, Nakamura T, Xuan Z, et al. A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J. 2010; 29: 3082–3093. PMC2944070 doi: 10.1038/emboj.2010.199 20729808

67. Chen B, Li S, Ren Q, Tong X, Zhang X, Kang L. Paternal epigenetic effects of population density on locust phase-related characteristics associated with heat-shock protein expression. Mol Ecol. 2015; 24: 851–862. doi: 10.1111/mec.13072 25581246

68. Chen S, Yang P, Jiang F, Wei Y, Ma Z, Kang L. De novo analysis of transcriptome dynamics in the migratory locust during the development of phase traits. PLoS One. 2010; 5: e15633. doi: 10.1371/journal.pone.0015633 21209894

69. Burns MJ, Nixon GJ, Foy CA, Harris N. Standardisation of data from real-time quantitative PCR methods–evaluation of outliers and comparison of calibration curves. BMC Biotechnol. 2005; 5: 31. doi: 10.1186/1472-6750-5-31 16336641

70. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998; 391: 806–811. doi: 10.1038/35888 9486653

71. Belles X. Beyond Drosophila: RNAi in vivo and functional genomics in insects. Annu Rev Entomol. 2010; 55: 111–128. doi: 10.1146/annurev-ento-112408-085301 19961326

72. Luo Y, Wang X, Yu D, Kang L. The SID-1 double-stranded RNA transporter is not required for systemic RNAi in the migratory locust. RNA Biol. 2012; 9: 663–671. doi: 10.4161/rna.19986 22614832

73. He J, Chen Q, Wei Y, Jiang F, Yang M, Hao S, et al. MicroRNA-276 promotes egg-hatching synchrony by up-regulating brm in locusts. Proc Natl Acad Sci USA. 2016; 113: 584–589. doi: 10.1073/pnas.1521098113 26729868

74. Wang Y, Yang P, Cui F, Kang L. Altered immunity in crowded locust reduced fungal (Metarhizium anisopliae) pathogenesis. PLoS Pathog. 2013; 9: e1003102. doi: 10.1371/journal.ppat.1003102 23326229

75. Hirosawa M, Hoshida M, Ishikawa M, Toya T. MASCOT: Multiple alignment system for protein sequences based on three-way dynamic programming. Bioinformatics. 1993; 9: 161–167. doi: 10.1093/bioinformatics/9.2.161 8481818

76. Wang X, Fang X, Yang P, Jiang X, Jiang F, Zhao D, et al. The locust genome provides insight into swarm formation and long-distance flight. Nat Commun. 2014; 5: 2957. doi: 10.1038/ncomms3957 24423660

77. Daubner GM, Cléry A, Jayne S, Stevenin J, Allain FHT. A syn–anti conformational difference allows SRSF2 to recognize guanines and cytosines equally well. EMBO J. 2012; 31: 162–174. doi: 10.1038/emboj.2011.367 22002536


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