-
Články
Top novinky
Reklama- Vzdělávání
- Časopisy
Top články
Nové číslo
- Témata
Top novinky
Reklama- Kongresy
- Videa
- Podcasty
Nové podcasty
Reklama- Kariéra
Doporučené pozice
Reklama- Praxe
Top novinky
ReklamaDrosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69
Autoři: Yasuko Kitatani aff001; Akane Tezuka aff001; Eri Hasegawa aff001; Satoyoshi Yanagi aff001; Kazuya Togashi aff001; Masato Tsuji aff001; Shu Kondo aff002; Jay Z. Parrish aff003; Kazuo Emoto aff001
Působiště autorů: Department of Biological Sciences, Graduate School of Science, University of Tokyo, Hongo, Bunkyo-ku, Tokyo, Japan aff001; Genetic Strains Research Center, National Institute of Genetics, Yata, Mishima, Shizuoka, Japan aff002; Department of Biology, University of Washington, Seattle, Washington, United States of America aff003; International Research Center for Neurointelligence (WPI-IRCN), University of Tokyo, Hongo, Bunkyo-ku, Tokyo, Japan aff004
Vyšlo v časopise: Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69. PLoS Genet 16(8): e32767. doi:10.1371/journal.pgen.1008942
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008942Souhrn
To remodel functional neuronal connectivity, neurons often alter dendrite arbors through elimination and subsequent regeneration of dendritic branches. However, the intrinsic mechanisms underlying this developmentally programmed dendrite regeneration and whether it shares common machinery with injury-induced regeneration remain largely unknown. Drosophila class IV dendrite arborization (C4da) sensory neurons regenerate adult-specific dendrites after eliminating larval dendrites during metamorphosis. Here we show that the microRNA miR-87 is a critical regulator of dendrite regeneration in Drosophila. miR-87 knockout impairs dendrite regeneration after developmentally-programmed pruning, whereas miR-87 overexpression in C4da neurons leads to precocious initiation of dendrite regeneration. Genetic analyses indicate that the transcriptional repressor Tramtrack69 (Ttk69) is a functional target for miR-87-mediated repression as ttk69 expression is increased in miR-87 knockout neurons and reducing ttk69 expression restores dendrite regeneration to mutants lacking miR-87 function. We further show that miR-87 is required for dendrite regeneration after acute injury in the larval stage, providing a mechanistic link between developmentally programmed and injury-induced dendrite regeneration. These findings thus indicate that miR-87 promotes dendrite regrowth during regeneration at least in part through suppressing Ttk69 in Drosophila sensory neurons and suggest that developmental and injury-induced dendrite regeneration share a common intrinsic mechanism to reactivate dendrite growth.
Klíčová slova:
Developmental neuroscience – Larvae – MicroRNAs – Neuronal dendrites – Neurons – Sensory perception – Nerve regeneration – Regeneration
Zdroje
1. Takeo YH, Kakegawa W, Miura E, Yuzaki M (2015) RORα regulates multiple aspects of dendrite development in cerebellar Purkinje cells in vivo. J Neurosci 35 : 12518–12534. doi: 10.1523/JNEUROSCI.0075-15.2015 26354918
2. Mizuno H, et al. (2014) NMDA-regulated dynamics of layer 4 neuronal dendrites during thalamocortical reorganization in neonates. Neuron 82 : 365–379. doi: 10.1016/j.neuron.2014.02.026 24685175
3. Nakazawa S, Mizuno H, Iwasato T (2018) Different dynamics of cortical neuron dendrite trees revealed by long-term in vivo imaging in neonates. Nat Commun 9 : 3106. doi: 10.1038/s41467-018-05563-0 30082783
4. Emoto K, Parrish JZ, Jan LY, Jan YN (2006) The tumour suppressor Hippo acts with the NDR kinases in dendrite tiling and maintenance. Nature 443 : 210–213. doi: 10.1038/nature05090 16906135
5. Parrish JZ, Emoto K, Jan LY, Jan YN (2007) Polycomb genes interact with the tumor suppressor genes hippo and warts in the maintenance of Drosophila sensory neuron dendrites. Genes Dev 21 : 956–972. doi: 10.1101/gad.1514507 17437999
6. Koleske AJ. (2013) Molecular mechanisms of dendrite stability. Nat Rev Neurosci 14 : 536–550. doi: 10.1038/nrn3486 23839597
7. Murphy TH, Corbett D (2009) Plasticity during stroke recovery: from synapse to behavior. Nat Rev Neurosci 10 : 861–872. doi: 10.1038/nrn2735 19888284
8. Ruan YWR, et al. (2006) Dendritic plasticity of CA1 pyramidal neurons after transient grobal ischemia. Neuroscience 140 : 191–201. doi: 10.1016/j.neuroscience.2006.01.039 16529877
9. Spigelman I, Yan XX, Obenaus A, Lee EY, Wasterlain CG, Ribak CE (1998) Dentate granule cells form novel basal dendrites in a rat model of temporal lobe epilepsy. Neuroscience 86 : 109–120. doi: 10.1016/s0306-4522(98)00028-1 9692747
10. Jan YN, Jan LY (2010) Branching out: mechanisms of dendrite arborization. Nat Rev Neurosci 11 : 316–328. doi: 10.1038/nrn2836 20404840
11. Yu F, Schuldiner O (2014) Axon and dendrite pruning in Drosophila. Curr Opin Neurobiol 27 : 192–198. doi: 10.1016/j.conb.2014.04.005 24793180
12. Kanamori T, Togashi K, Koizumi H, Emoto K (2015) Dendrite remodeling: lessons from invertebrate models. Int Rev Cell Mol Biol 318 : 1–15. doi: 10.1016/bs.ircmb.2015.05.001 26315882
13. Kuo CT, Jan LY, Jan YN (2005) Dendrite-specific remodeling of Drosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteasome, and ecdysone signaling. Proc Natl Acad Sci USA 102 : 15230–15235. doi: 10.1073/pnas.0507393102 16210248
14. Williams DW, Truman JW (2005) Remodeling dendrites during insect metamorphosis. J Neurobiol 64 : 24–33. doi: 10.1002/neu.20151 15884009
15. Kanamori T, Kanai MI, Dairyo Y, Yasunaga KI, Morikawa RK, Emoto K (2013) Compartmentalized calcium transients trigger dendrite pruning in Drosophila sensory neurons. Science 340 : 1475–1478. doi: 10.1126/science.1234879 23722427
16. Shimono K, et al. (2009) Multidendritic sensory neurons in the adult Drosophila abdomen: origin, dendritic morphology, and segment - and age-dependent programmed cell death. Neural Dev 4 : 37. doi: 10.1186/1749-8104-4-37 19799768
17. Yasunaga KI, Kanamori T, Morikawa R, Emoto K (2010) Dendrite reshaping of adult Drosophila sensory neurons requires matrix metalloproteinase - mediated modification of the basement membranes. Dev Cell 18 : 621–632. doi: 10.1016/j.devcel.2010.02.010 20412776
18. Yasunaga KI, et al. (2015) Adult Drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the Wnt5-Drl signaling pathway. Genes Dev 29 : 1763–1775. doi: 10.1101/gad.262592.115 26302791
19. Lyons GR, Anderson RO, Abdi K, Song WS, Kuo CT (2014) Cysteine proteinase-1 and cut protein isoform control dendritic innervation of two distinct sensory fields by a single neuron. Cell Rep 6 : 783–791. doi: 10.1016/j.celrep.2014.02.003 24582961
20. Song Y, Ori-McKenney KM, Zheng Y, Han C, Jan LY, Jan YN (2012) Regeneration of Drosophila sensory neuron axons and dendrites is regulated by the AKT pathway involving Pten and microRNA bantam. Genes Dev 26 : 1612–1625. doi: 10.1101/gad.193243.112 22759636
21. Stone MC, Albertson RM, Chen L, Rolls MM (2014) Dendrite injury triggers DLK-independent regeneration. Cell Rep 6 : 247–253. doi: 10.1016/j.celrep.2013.12.022 24412365
22. Thompson-Peer K, DeVault L, Li T, Jan LY, Jan YN (2016) In vivo dendrite regeneration after injury is different from dendrite development. Genes Dev 30 : 1776–1789. doi: 10.1101/gad.282848.116 27542831
23. Devaut L, Li T, Izabel S, Thompson-Peer K, Jan LY, Jan YN (2018) Dendrite regeneration of adult Drosophila sensory neurons diminishes with aging and is inhibited by epidermal-derived matrix metalloproteinase 2. Genes Dev 32 : 402–414. doi: 10.1101/gad.308270.117 29563183
24. Chang S, Johnstone RJ, Frokjer-Jensen C, Lockery S, Hobert O (2004) MicroRNAs act sequentially and asymmetrically to control chemosensory laterality in the nematode. Nature 430 : 785–789. doi: 10.1038/nature02752 15306811
25. Zou Y, Chiu H, Domenger D, Chuang CF, Chang C (2012) The lin-4 microRNA targets the LIN-14 transcription factor to inhibit Netrin-mediated axon attraction. Sci Signal 5: ra43. doi: 10.1126/scisignal.2002437 22692424
26. Sun AX, Crabtree GR, Yoo AS (2013) MicroRNAs: regulations of neuronal fate. Curr Opin Cell Biol 25 : 215–221. doi: 10.1016/j.ceb.2012.12.007 23374323
27. Shenoy A, Blelloch RH (2014) Regulation of microRNA function in somatic stem cell proliferation and differentiation. Nat Rev Mol Cell Biol 15 : 565–576. doi: 10.1038/nrm3854 25118717
28. Guo H, Ingolia NT, Weissman JS, Bartel DP (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466 : 835–840. doi: 10.1038/nature09267 20703300
29. Djuranovic S, Nahvi A, Green R (2012) miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336 : 237–240. doi: 10.1126/science.1215691 22499947
30. Ghibaudi M, Boido M, Vercelli A (2017) Functional integration of complex miRNA networks in central and peripheral lesion and axonal regeneration. Prog Neurobiol 158 : 69–93. doi: 10.1016/j.pneurobio.2017.07.005 28779869
31. Mahar M, Cavalli V (2018) Intrinsic mechanisms of neuronal axon regeneration. Nat Rev Neurosci 19 : 323–337. doi: 10.1038/s41583-018-0001-8 29666508
32. Gaudet AD, et al. (2016) miR-155 deletion in mice overcomes neuron-intrinsic and neuron-extrinsic barriers to spinal cord repair. J Neurosci 36 : 8516–8532. doi: 10.1523/JNEUROSCI.0735-16.2016 27511021
33. Hu YW, Jiang JJ, Gao Y, Wang RY, Tu GJ (2016) MicroRNA-210 promotes sensory axon regeneration of adult mice in vivo and in vitro. Neurosci Lett 622 : 61–66. doi: 10.1016/j.neulet.2016.04.034 27102143
34. Yu YM, et al. (2011) MicroRNA miR-133b is essential for functional recovery after spinal cord injury in adult zebrafish. Eur J Neurosci 33 : 1587–1597 (2011). doi: 10.1111/j.1460-9568.2011.07643.x 21447094
35. Liu CM, Wang RY, Saijilafu, Jiao ZX, Zhang BY, Zhou FQ(2013) MicroRNA-138 and SIRT1 form a mutual negative feedback loop to regulate mammalian axon regeneration. Genes Dev 27 : 1473–1483. doi: 10.1101/gad.209619.112 23796896
36. Chen YW, et al. (2014) Systematic study of Drosophila microRNA functions using a collection of targeted knockout mutations. Dev Cell 31 : 784–800. doi: 10.1016/j.devcel.2014.11.029 25535920
37. Kanamori T, Yoshino J, Yasunaga KI, Dairyo Y, Emoto K (2015) Local endocytosis triggers dendritic thinning and pruning in Drosophila sensory neurons. Nat Commun 6 : 6515. doi: 10.1038/ncomms7515 25761586
38. Parrish JZ, Xu P, Kim CC, Jan LY, Jan YN (2009) The microRNA bantam functions in epithelial cells to regulate scaling growth of dendrite arbors in Drosophila sensory neurons. Neuron 63 : 788–802. doi: 10.1016/j.neuron.2009.08.006 19778508
39. Lee T, Luo L (1999) Mosaic analysis with repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22 : 451–461. doi: 10.1016/s0896-6273(00)80701-1 10197526
40. Sempere LF, Sokol NS, Dubrosky EB, Berger EM, Ambros V (2003) Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and broad-Complex gene activity. Dev Biol 259 : 9–18. doi: 10.1016/s0012-1606(03)00208-2 12812784
41. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM (2003) bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113 : 25–36. doi: 10.1016/s0092-8674(03)00231-9 12679032
42. Stark A, Brennecke J, Russell RB, Cohen SM (2003) Identification of Drosophila MicroRNA targets. PLoS Biol 1: E60. doi: 10.1371/journal.pbio.0000060 14691535
43. Huang YC, Smith L, Poulton J, Deng WM (2013) The microRNA miR-7 regulates Tramtrack69 in a developmental switch in Drosophila follicle cells. Development 140 : 897–905. doi: 10.1242/dev.080192 23325762
44. Xiong WC, Montell C (1993) tramtrack is a transcriptional repressor required for cell fate determination in the Drosophila eye. Genes Dev 7 : 1085–1096. doi: 10.1101/gad.7.6.1085 8504931
45. Guo M, Bier E, Jan LY, Jan YN (1995) tramtrack acts downstream of numb to specify distinct daughter cell fates during asymmetric cell divisions in the Drosophila PNS. Neuron 14 : 913–925. doi: 10.1016/0896-6273(95)90330-5 7748559
46. Li S, Li Y, Carthew RW, Lai ZC (1997) Photoreceptor cell differentiation requires regulated proteolysis of the transcriptional repressor Tramtrack. Cell 90 : 469–478. doi: 10.1016/s0092-8674(00)80507-3 9267027
47. Lai ZC, Li Y (1999) Tramtrack69 is positively and autonomously required for Drosophila photoreceptor development. Genetics 152 : 299–305. 10224262
48. Parrish JZ, Kim MD, Jan LY, Jan YN (2006) Genome-wide analyses identify transcription factors required for proper morphogenesis of Drosophila sensory neuron dendrites. Genes Dev 20 : 820–835. doi: 10.1101/gad.1391006 16547170
49. Kniss JS, Holbrook S, Mergman TG (2013) R7 photoreceptor axon growth is temporally controlled by the transcription factor Ttk69, which inhibits growth in part by promoting transforming growth factor-β/activin signaling. J Neurosci 33 : 1509–1520. doi: 10.1523/JNEUROSCI.2023-12.2013 23345225
50. Feoktistov AI, Herman TG (2016) Wallenda/DLK protein levels are temporally downregulated by Tramtrack69 to allow R7 growth cones to become stationary boutons. Development 143 : 2983–2993. doi: 10.1242/dev.134403 27402706
51. Iovino N, Pane A, Gaul U (2009) miR-184 has multiple roles in Drosophila female germline development. Dev Cell 17 : 123–133. doi: 10.1016/j.devcel.2009.06.008 19619497
52. Cicek IO, Karaca S, Brankatschk M, Eaton S, Urlaub H, Shcherbata HR (2016) Hedgehog signaling strength is orchestrated by the mir-310 cluster of microRNAs in response to diet. Genetics 202 : 1167–1183. doi: 10.1534/genetics.115.185371 26801178
53. Yamanaka N, Rewitz KF, O’Connor MB (2013) Ecdysone control of developmental transition: lessons from Drosophila research. Annu Rev Entomol 58 : 497–516. doi: 10.1146/annurev-ento-120811-153608 23072462
54. Handler AM (1982) Ecdysteroid titers during pupal and adult development in Drosophila melanogaster. Dev Biol 93 : 73–82. doi: 10.1016/0012-1606(82)90240-8 6813165
55. Thummel CS (2001) Molecular mechanisms of developmental timing in C. elegans and Drosophila. Dev Cell 4 : 453–465.
56. Cherbas L, Willingham A, Zhag D, Yang L, Zou Y, Eads BD, Carlson JW, Landolin JM, Kapranov P, Dumais J, Samsonova A, Choi JH, Roberts J, Davis C, Tang H, van Baren MJ, Ghosh S, Dobin A, Bell K, Lin W, Langton L, Duff MO, Tenney AE, Zaleski C, Brent MR, Hoskins RA, Kaufman TC, Andrews J, Gravely BR, Perrimon N, Celniker SE, Ginveras TR, and Cherbas P (2011) The transcriptional diversity of 25 Drosophila cell lines. Genome Res 2 : 301–314.
Článek A point mutation decouples the lipid transfer activities of microsomal triglyceride transfer proteinČlánek A human-specific VNTR in the TRIB3 promoter causes gene expression variation between individualsČlánek Phospho-regulation of the Shugoshin - Condensin interaction at the centromere in budding yeastČlánek Costly GenesČlánek The roles of replication-transcription conflict in mutagenesis and evolution of genome organization
Článek vyšel v časopisePLOS Genetics
Nejčtenější tento týden
2020 Číslo 8- Ukažte mi, jak kašlete, a já vám řeknu, co vám je
- Test BioCog: 10 minut k orientaci v kognitivním stavu pacienta
- VIDEO: Terénní tým ECMO zachraňuje životy přímo v pražských ulicích
- Alkohol, zima a léky − sezónní rizika interakcí
- „Jednohubky“ z výzkumu 2025/40 – vánoční a silvestrovská porce
-
Všechny články tohoto čísla
- Demographic history shaped geographical patterns of deleterious mutation load in a broadly distributed Pacific Salmon
- Immediate activation of chemosensory neuron gene expression by bacterial metabolites is selectively induced by distinct cyclic GMP-dependent pathways in Caenorhabditis elegans
- Phospho-regulation of the Shugoshin - Condensin interaction at the centromere in budding yeast
- Gα/GSA-1 works upstream of PKA/KIN-1 to regulate calcium signaling and contractility in the Caenorhabditis elegans spermatheca
- Mutation of CFAP57, a protein required for the asymmetric targeting of a subset of inner dynein arms in Chlamydomonas, causes primary ciliary dyskinesia
- Uptake of exogenous serine is important to maintain sphingolipid homeostasis in Saccharomyces cerevisiae
- Transcriptional regulators of the Golli/myelin basic protein locus integrate additive and stealth activities
- Conditional antagonism in co-cultures of Pseudomonas aeruginosa and Candida albicans: An intersection of ethanol and phosphate signaling distilled from dual-seq transcriptomics
- DAnkrd49 and Bdbt act via Casein kinase Iε to regulate planar polarity in Drosophila
- Costly Genes
- Hypomodified tRNA in evolutionarily distant yeasts can trigger rapid tRNA decay to activate the general amino acid control response, but with different consequences
- Mapping gene flow between ancient hominins through demography-aware inference of the ancestral recombination graph
- Learning the properties of adaptive regions with functional data analysis
- Epistatic interactions between killer immunoglobulin-like receptors and human leukocyte antigen ligands are associated with ankylosing spondylitis
- Endogenization and excision of human herpesvirus 6 in human genomes
- A subset of broadly responsive Type III taste cells contribute to the detection of bitter, sweet and umami stimuli
- On the cross-population generalizability of gene expression prediction models
- How many familial relationship testing results could be wrong?
- Long noncoding RNA functionality in imprinted domain regulation
- Horizontal transmission and recombination maintain forever young bacterial symbiont genomes
- A point mutation decouples the lipid transfer activities of microsomal triglyceride transfer protein
- Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69
- A general framework for functionally informed set-based analysis: Application to a large-scale colorectal cancer study
- THOC1 deficiency leads to late-onset nonsyndromic hearing loss through p53-mediated hair cell apoptosis
- Cfap97d1 is important for flagellar axoneme maintenance and male mouse fertility
- Disruption of the ERLIN–TM6SF2–APOB complex destabilizes APOB and contributes to non-alcoholic fatty liver disease
- Haspin kinase modulates nuclear architecture and Polycomb-dependent gene silencing
- Mushroom body subsets encode CREB2-dependent water-reward long-term memory in Drosophila
- Replication of the Salmonella Genomic Island 1 (SGI1) triggered by helper IncC conjugative plasmids promotes incompatibility and plasmid loss
- Nitrogen coordinated import and export of arginine across the yeast vacuolar membrane
- Paired Box 9 (PAX9), the RNA polymerase II transcription factor, regulates human ribosome biogenesis and craniofacial development
- Genomic imprinting: An epigenetic regulatory system
- Leveraging a gain-of-function allele of Caenorhabditis elegans paqr-1 to elucidate membrane homeostasis by PAQR proteins
- Sequential activation of Notch and Grainyhead gives apoptotic competence to Abdominal-B expressing larval neuroblasts in Drosophila Central nervous system
- Systematic identification of functional SNPs interrupting 3’UTR polyadenylation signals
- A human-specific VNTR in the TRIB3 promoter causes gene expression variation between individuals
- Gluconeogenesis and PEPCK are critical components of healthy aging and dietary restriction life extension
- Natural variation in a glucuronosyltransferase modulates propionate sensitivity in a C. elegans propionic acidemia model
- The roles of replication-transcription conflict in mutagenesis and evolution of genome organization
- Distinct and sequential re-replication barriers ensure precise genome duplication
- Drosophila Myc restores immune homeostasis of Imd pathway via activating miR-277 to inhibit imd/Tab2
- Polo kinase recruitment via the constitutive centromere-associated network at the kinetochore elevates centromeric RNA
- Cryptic genetic variation enhances primate L1 retrotransposon survival by enlarging the functional coiled coil sequence space of ORF1p
- Quorum sensing sets the stage for the establishment and vertical transmission of Sodalis praecaptivus in tsetse flies
- Pan-genomic open reading frames: A potential supplement of single nucleotide polymorphisms in estimation of heritability and genomic prediction
- The High Osmolarity Glycerol Mitogen-Activated Protein Kinase regulates glucose catabolite repression in filamentous fungi
- Serotonergic modulation of visual neurons in Drosophila melanogaster
- Functional information from clinically-derived drug resistant forms of the Candida glabrata Pdr1 transcription factor
- PLOS Genetics
- Archiv čísel
- Aktuální číslo
- Informace o časopisu
Nejčtenější v tomto čísle- Genomic imprinting: An epigenetic regulatory system
- A human-specific VNTR in the TRIB3 promoter causes gene expression variation between individuals
- Uptake of exogenous serine is important to maintain sphingolipid homeostasis in Saccharomyces cerevisiae
- A point mutation decouples the lipid transfer activities of microsomal triglyceride transfer protein
Kurzy
Zvyšte si kvalifikaci online z pohodlí domova
Autoři: prof. MUDr. Vladimír Palička, CSc., Dr.h.c., doc. MUDr. Václav Vyskočil, Ph.D., MUDr. Petr Kasalický, CSc., MUDr. Jan Rosa, Ing. Pavel Havlík, Ing. Jan Adam, Hana Hejnová, DiS., Jana Křenková
Autoři: MUDr. Irena Krčmová, CSc.
Autoři: MDDr. Eleonóra Ivančová, PhD., MHA
Autoři: prof. MUDr. Eva Kubala Havrdová, DrSc.
Všechny kurzyPřihlášení#ADS_BOTTOM_SCRIPTS#Zapomenuté hesloZadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.
- Vzdělávání