#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Mmp1 Processing of the PDF Neuropeptide Regulates Circadian Structural Plasticity of Pacemaker Neurons


Circadian clocks have evolved as mechanisms that allow organisms to adapt to the day/night cyclical changes, a direct consequence of the rotation of the Earth. In the last two decades, and due to its amazing repertoire of genetic tools, Drosophila has been at the leading front in the discovery of genes that account for how the clock operates at a single cell level, which are conserved throughout the animal kingdom. Although the biochemical components underlying these molecular clocks have been characterized in certain detail, the mechanisms used by clock neurons to convey information to downstream pathways controlling behavior remain elusive. In the fruit fly, a subset of circadian neurons called the small ventral lateral neurons (sLNvs) are capable of synchronizing other clock cells relying on a neuropeptide named pigment dispersing factor (PDF). In addition, a number of years ago we described another mechanism as a possible candidate for contributing to the transmission of information downstream of the sLNvs, involving adult-specific remodeling of the axonal terminals of these circadian neurons. In this manuscript we describe some of the molecular events that lead to this striking form of structural plasticity on a daily basis.


Vyšlo v časopise: Mmp1 Processing of the PDF Neuropeptide Regulates Circadian Structural Plasticity of Pacemaker Neurons. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004700
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004700

Souhrn

Circadian clocks have evolved as mechanisms that allow organisms to adapt to the day/night cyclical changes, a direct consequence of the rotation of the Earth. In the last two decades, and due to its amazing repertoire of genetic tools, Drosophila has been at the leading front in the discovery of genes that account for how the clock operates at a single cell level, which are conserved throughout the animal kingdom. Although the biochemical components underlying these molecular clocks have been characterized in certain detail, the mechanisms used by clock neurons to convey information to downstream pathways controlling behavior remain elusive. In the fruit fly, a subset of circadian neurons called the small ventral lateral neurons (sLNvs) are capable of synchronizing other clock cells relying on a neuropeptide named pigment dispersing factor (PDF). In addition, a number of years ago we described another mechanism as a possible candidate for contributing to the transmission of information downstream of the sLNvs, involving adult-specific remodeling of the axonal terminals of these circadian neurons. In this manuscript we describe some of the molecular events that lead to this striking form of structural plasticity on a daily basis.


Zdroje

1. HutRA, BeersmaDG (2011) Evolution of time-keeping mechanisms: early emergence and adaptation to photoperiod. Philos Trans R Soc Lond B Biol Sci 366: 2141–2154.

2. OzkayaO, RosatoE (2012) The circadian clock of the fly: a neurogenetics journey through time. Adv Genet 77: 79–123.

3. FrenkelL, CerianiMF (2011) Circadian plasticity: from structure to behavior. Int Rev Neurobiol 99: 107–138.

4. Helfrich-ForsterC, ShaferOT, WulbeckC, GrieshaberE, RiegerD, et al. (2007) Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J Comp Neurol 500: 47–70.

5. RennSC, ParkJH, RosbashM, HallJC, TaghertPH (1999) A pdf neuropeptide gene mutation and ablation of PDF neurons each cause severe abnormalities of behavioral circadian rhythms in Drosophila. Cell 99: 791–802.

6. GrimaB, ChelotE, XiaR, RouyerF (2004) Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431: 869–873.

7. StoleruD, PengY, AgostoJ, RosbashM (2004) Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431: 862–868.

8. SheebaV, FogleKJ, KanekoM, RashidS, ChouYT, et al. (2008) Large ventral lateral neurons modulate arousal and sleep in Drosophila. Curr Biol 18: 1537–1545.

9. PariskyKM, AgostoJ, PulverSR, ShangY, KuklinE, et al. (2008) PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60: 672–682.

10. ShangY, GriffithLC, RosbashM (2008) Light-arousal and circadian photoreception circuits intersect at the large PDF cells of the Drosophila brain. Proc Natl Acad Sci U S A 105: 19587–19594.

11. LinY, StormoGD, TaghertPH (2004) The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J Neurosci 24: 7951–7957.

12. ParkJH, Helfrich-ForsterC, LeeG, LiuL, RosbashM, et al. (2000) Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. ProcNatlAcadSciUSA 97: 3608–3613.

13. CaoG, NitabachMN (2008) Circadian control of membrane excitability in Drosophila melanogaster lateral ventral clock neurons. J Neurosci 28: 6493–6501.

14. FernandezMP, BerniJ, CerianiMF (2008) Circadian remodeling of neuronal circuits involved in rhythmic behavior. PLoS Biol 6: e69.

15. GorostizaEA, Depetris-ChauvinA, FrenkelL, PírezN, CerianiMF (2014) Circadian pacemaker neurons change synaptic contacts across the day. Curr Biol 24: 1–7.

16. De PaolaV, HoltmaatA, KnottG, SongS, WilbrechtL, et al. (2006) Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron 49: 861–875.

17. MajewskaAK, NewtonJR, SurM (2006) Remodeling of synaptic structure in sensory cortical areas in vivo. J Neurosci 26: 3021–3029.

18. GogollaN, GalimbertiI, CaroniP (2007) Structural plasticity of axon terminals in the adult. Curr Opin Neurobiol 17: 516–524.

19. AppelbaumL, WangG, YokogawaT, SkariahGM, SmithSJ, et al. (2010) Circadian and homeostatic regulation of structural synaptic plasticity in hypocretin neurons. Neuron 68: 87–98.

20. BusheyD, TononiG, CirelliC (2011) Sleep and synaptic homeostasis: structural evidence in Drosophila. Science 332: 1576–1581.

21. MehnertKI, BeramendiA, ElghazaliF, NegroP, KyriacouCP, et al. (2007) Circadian changes in Drosophila motor terminals. Dev Neurobiol 67: 415–421.

22. BarthM, SchultzeM, SchusterCM, StraussR (2010) Circadian plasticity in photoreceptor cells controls visual coding efficiency in Drosophila melanogaster. PLoS One 5: e9217.

23. BecquetD, GirardetC, GuillaumondF, Francois-BellanAM, BoslerO (2008) Ultrastructural plasticity in the rat suprachiasmatic nucleus. Possible involvement in clock entrainment. Glia 56: 294–305.

24. Page-McCawA, SeranoJ, SanteJM, RubinGM (2003) Drosophila matrix metalloproteinases are required for tissue remodeling, but not embryonic development. Dev Cell 4: 95–106.

25. BeaucherM, HerspergerE, Page-McCawA, ShearnA (2007) Metastatic ability of Drosophila tumors depends on MMP activity. Dev Biol 303: 625–634.

26. MillerCM, Page-McCawA, BroihierHT (2008) Matrix metalloproteinases promote motor axon fasciculation in the Drosophila embryo. Development 135: 95–109.

27. KuoCT, JanLY, JanYN (2005) Dendrite-specific remodeling of Drosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteasome, and ecdysone signaling. Proc Natl Acad Sci U S A 102: 15230–15235.

28. NagoshiE, SuginoK, KulaE, OkazakiE, TachibanaT, et al. (2010) Dissecting differential gene expression within the circadian neuronal circuit of Drosophila. Nat Neurosci 13: 60–68.

29. KadenerS, StoleruD, McDonaldM, NawatheanP, RosbashM (2007) Clockwork Orange is a transcriptional repressor and a new Drosophila circadian pacemaker component. Genes Dev 21: 1675–1686.

30. Depetris-ChauvinA, BerniJ, AranovichEJ, MuraroNI, BeckwithEJ, et al. (2011) Adult-specific electrical silencing of pacemaker neurons uncouples molecular clock from circadian outputs. Curr Biol 21: 1783–1793.

31. Kula-EversoleE, NagoshiE, ShangY, RodriguezJ, AlladaR, et al. (2010) Surprising gene expression patterns within and between PDF-containing circadian neurons in Drosophila. Proc Natl Acad Sci U S A 107: 13497–13502.

32. SivachenkoA, LiY, AbruzziKC, RosbashM (2013) The transcription factor mef2 links the Drosophila core clock to fas2, neuronal morphology, and circadian behavior. Neuron 79: 281–292.

33. GorostizaEA, CerianiMF (2013) Retrograde bone morphogenetic protein signaling shapes a key circadian pacemaker circuit. J Neurosci 33: 687–696.

34. LearBC, MerrillCE, LinJM, SchroederA, ZhangL, et al. (2005) A G protein-coupled receptor, groom-of-PDF, is required for PDF neuron action in circadian behavior. Neuron 48: 221–227.

35. HyunS, LeeY, HongST, BangS, PaikD, et al. (2005) Drosophila GPCR Han is a receptor for the circadian clock neuropeptide PDF. Neuron 48: 267–278.

36. HusainQM, EwerJ (2004) Use of targetable gfp-tagged neuropeptide for visualizing neuropeptide release following execution of a behavior. J Neurobiol 59: 181–191.

37. RaoS, LangC, LevitanES, DeitcherDL (2001) Visualization of neuropeptide expression, transport, and exocytosis in Drosophila melanogaster. J Neurobiol 49: 159–172.

38. LlanoE, PendasAM, Aza-BlancP, KornbergTB, Lopez-OtinC (2000) Dm1-MMP, a matrix metalloproteinase from Drosophila with a potential role in extracellular matrix remodeling during neural development. J Biol Chem 275: 35978–35985.

39. IsaacRE, JohnsonEC, AudsleyN, ShirrasAD (2007) Metabolic inactivation of the circadian transmitter, pigment dispersing factor (PDF), by neprilysin-like peptidases in Drosophila. J Exp Biol 210: 4465–4470.

40. SledgeGWJr, QulaliM, GouletR, BoneEA, FifeR (1995) Effect of matrix metalloproteinase inhibitor batimastat on breast cancer regrowth and metastasis in athymic mice. J Natl Cancer Inst 87: 1546–1550.

41. ParkJH, HallJC (1998) Isolation and chronobiological analysis of a neuropeptide pigment- dispersing factor gene in Drosophila melanogaster. JBiolRhythms 13: 219–228.

42. LlanoE, AdamG, PendasAM, QuesadaV, SanchezLM, et al. (2002) Structural and enzymatic characterization of Drosophila Dm2-MMP, a membrane-bound matrix metalloproteinase with tissue-specific expression. J Biol Chem 277: 23321–23329.

43. Helfrich-ForsterC, TauberM, ParkJH, Muhlig-VersenM, SchneuwlyS, et al. (2000) Ectopic expression of the neuropeptide pigment-dispersing factor alters behavioral rhythms in Drosophila melanogaster. JNeurosci 20: 3339–3353.

44. WulbeckC, GrieshaberE, Helfrich-ForsterC (2008) Pigment-dispersing factor (PDF) has different effects on Drosophila's circadian clocks in the accessory medulla and in the dorsal brain. J Biol Rhythms 23: 409–424.

45. SheebaV, SharmaVK, GuH, ChouYT, O'DowdDK, et al. (2008) Pigment dispersing factor-dependent and -independent circadian locomotor behavioral rhythms. JNeurosci 28: 217–227.

46. YoshiiT, WulbeckC, SehadovaH, VeleriS, BichlerD, et al. (2009) The neuropeptide pigment-dispersing factor adjusts period and phase of Drosophila's clock. J Neurosci 29: 2597–2610.

47. ShaferOT, KimDJ, Dunbar-YaffeR, NikolaevVO, LohseMJ, et al. (2008) Widespread receptivity to neuropeptide PDF throughout the neuronal circadian clock network of Drosophila revealed by real-time cyclic AMP imaging. Neuron 58: 223–237.

48. DuvallLB, TaghertPH (2012) The circadian neuropeptide PDF signals preferentially through a specific adenylate cyclase isoform AC3 in M pacemakers of Drosophila. PLoS Biol 10: e1001337.

49. PengY, StoleruD, LevineJD, HallJC, RosbashM (2003) Drosophila free-running rhythms require intercellular communication. PLoS Biol 1: E13.

50. MillerCM, LiuN, Page-McCawA, BroihierHT (2011) Drosophila MMP2 regulates the matrix molecule faulty attraction (Frac) to promote motor axon targeting in Drosophila. J Neurosci 31: 5335–5347.

51. YasunagaK, KanamoriT, MorikawaR, SuzukiE, EmotoK (2010) Dendrite reshaping of adult Drosophila sensory neurons requires matrix metalloproteinase-mediated modification of the basement membranes. Dev Cell 18: 621–632.

52. SillerSS, BroadieK (2011) Neural circuit architecture defects in a Drosophila model of Fragile X syndrome are alleviated by minocycline treatment and genetic removal of matrix metalloproteinase. Dis Model Mech 4: 673–685.

53. Meyer-BernsteinEL, JettonAE, MatsumotoSI, MarkunsJF, LehmanMN, et al. (1999) Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology 140: 207–218.

54. SilverR, LeSauterJ, TrescoPA, LehmanMN (1996) A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms. Nature 382: 810–813.

55. de la IglesiaHO, SchwartzWJ (2006) Minireview: timely ovulation: circadian regulation of the female hypothalamo-pituitary-gonadal axis. Endocrinology 147: 1148–1153.

56. Birkedal-HansenH, MooreWG, BoddenMK, WindsorLJ, Birkedal-HansenB, et al. (1993) Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 4: 197–250.

57. KadenerS, MenetJS, SuginoK, HorwichMD, WeissbeinU, et al. (2009) A role for microRNAs in the Drosophila circadian clock. Genes Dev 23: 2179–2191.

58. RodriguezJ, TangCH, KhodorYL, VodalaS, MenetJS, et al. (2013) Nascent-Seq analysis of Drosophila cycling gene expression. Proc Natl Acad Sci U S A 110: E275–284.

59. SternlichtMD, WerbZ (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17: 463–516.

60. ChoiC, CaoG, TanenhausAK, McCarthyEV, JungM, et al. (2012) Autoreceptor control of peptide/neurotransmitter corelease from PDF neurons determines allocation of circadian activity in drosophila. Cell Rep 2: 332–344.

61. BeckwithEJ, GorostizaEA, BerniJ, RezavalC, Perez-SantangeloA, et al. (2013) Circadian Period Integrates Network Information Through Activation of the BMP Signaling Pathway. PLoS Biol 11: e1001733.

62. SheebaV, GuH, SharmaVK, O'DowdDK, HolmesTC (2008) Circadian- and light-dependent regulation of resting membrane potential and spontaneous action potential firing of Drosophila circadian pacemaker neurons. JNeurophysiol 99: 976–988.

63. RestituitoS, KhatriL, NinanI, MathewsPM, LiuX, et al. (2011) Synaptic autoregulation by metalloproteases and gamma-secretase. J Neurosci 31: 12083–12093.

64. DziembowskaM, WlodarczykJ (2012) MMP9: a novel function in synaptic plasticity. Int J Biochem Cell Biol 44: 709–713.

65. UhlirovaM, BohmannD (2006) JNK- and Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila. EMBO J 25: 5294–5304.

66. CerianiMF, HogeneschJB, YanovskyM, PandaS, StraumeM, et al. (2002) Genome-wide expression analysis in Drosophila reveals genes controlling circadian behavior. J Neurosci 22: 9305–9319.

67. IsaacRE, NasselDR (2003) Identification and localization of a neprilysin-like activity that degrades tachykinin-related peptides in the brain of the cockroach, Leucophaea maderae, and locust, Locusta migratoria. J Comp Neurol 457: 57–66.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#