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Sensory Neurons Arouse . Locomotion via Both Glutamate and Neuropeptide Release


Animals switch between periods of behavioral arousal and quiescence in response to environmental, developmental, and circadian cues. Little is known about the circuit mechanisms that produce these behavioral states. During larval molts, C. elegans exhibits a sleep-like state (termed lethargus) that is characterized by the absence of feeding and profound locomotion quiescence. We previously showed that mutants lacking the neuropeptide receptor NPR-1 exhibit increased arousal during larval molts, which is in part mediated by increased secretion of an arousal peptide (PDF-1). Here, we compare the circuits regulating arousal in larval molts and adults. We show that a broad network of sensory neurons arouses locomotion but that the impact of each neuron differs between lethargus and adults. We propose that this broad sensory network allows C. elegans to adapt its behavior across a broad range of developmental and physiological circumstances.


Vyšlo v časopise: Sensory Neurons Arouse . Locomotion via Both Glutamate and Neuropeptide Release. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005359
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005359

Souhrn

Animals switch between periods of behavioral arousal and quiescence in response to environmental, developmental, and circadian cues. Little is known about the circuit mechanisms that produce these behavioral states. During larval molts, C. elegans exhibits a sleep-like state (termed lethargus) that is characterized by the absence of feeding and profound locomotion quiescence. We previously showed that mutants lacking the neuropeptide receptor NPR-1 exhibit increased arousal during larval molts, which is in part mediated by increased secretion of an arousal peptide (PDF-1). Here, we compare the circuits regulating arousal in larval molts and adults. We show that a broad network of sensory neurons arouses locomotion but that the impact of each neuron differs between lethargus and adults. We propose that this broad sensory network allows C. elegans to adapt its behavior across a broad range of developmental and physiological circumstances.


Zdroje

1. Pfaff D, Ribeiro A, Matthews J, Kow LM (2008) Concepts and mechanisms of generalized central nervous system arousal. Annals of the New York Academy of Sciences 1129: 11–25. doi: 10.1196/annals.1417.019 18591465

2. Cirelli C (2009) The genetic and molecular regulation of sleep: from fruit flies to humans. Nature reviews Neuroscience 10: 549–560. doi: 10.1038/nrn2683 19617891

3. Cassada RC, Russell RL (1975) The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Developmental biology 46: 326–342. 1183723

4. Raizen DM, Zimmerman JE, Maycock MH, Ta UD, You YJ, et al. (2008) Lethargus is a Caenorhabditis elegans sleep-like state. Nature 451: 569–572. doi: 10.1038/nature06535 18185515

5. Van Buskirk C, Sternberg PW (2007) Epidermal growth factor signaling induces behavioral quiescence in Caenorhabditis elegans. Nature neuroscience 10: 1300–1307. 17891142

6. Singh K, Chao MY, Somers GA, Komatsu H, Corkins ME, et al. (2011) C. elegans Notch signaling regulates adult chemosensory response and larval molting quiescence. Current biology: CB 21: 825–834. doi: 10.1016/j.cub.2011.04.010 21549604

7. Monsalve GC, Van Buskirk C, Frand AR (2011) LIN-42/PERIOD controls cyclical and developmental progression of C. elegans molts. Current biology: CB 21: 2033–2045. doi: 10.1016/j.cub.2011.10.054 22137474

8. Turek M, Lewandrowski I, Bringmann H (2013) An AP2 transcription factor is required for a sleep-active neuron to induce sleep-like quiescence in C. elegans. Curr Biol 23: 2215–2223. doi: 10.1016/j.cub.2013.09.028 24184105

9. Nagy S, Wright C, Tramm N, Labello N, Burov S, et al. (2013) A longitudinal study of Caenorhabditis elegans larvae reveals a novel locomotion switch, regulated by Galphas signaling. Elife 2: e00782. doi: 10.7554/eLife.00782 23840929

10. Nelson MD, Trojanowski NF, George-Raizen JB, Smith CJ, Yu CC, et al. (2013) The neuropeptide NLP-22 regulates a sleep-like state in Caenorhabditis elegans. Nat Commun 4: 2846. doi: 10.1038/ncomms3846 24301180

11. Choi S, Chatzigeorgiou M, Taylor KP, Schafer WR, Kaplan JM (2013) Analysis of NPR-1 reveals a circuit mechanism for behavioral quiescence in C. elegans. Neuron 78: 869–880. doi: 10.1016/j.neuron.2013.04.002 23764289

12. Cho JY, Sternberg PW (2014) Multilevel modulation of a sensory motor circuit during C. elegans sleep and arousal. Cell 156: 249–260. doi: 10.1016/j.cell.2013.11.036 24439380

13. Schwarz J, Lewandrowski I, Bringmann H (2011) Reduced activity of a sensory neuron during a sleep-like state in Caenorhabditis elegans. Current biology: CB 21: R983–984. doi: 10.1016/j.cub.2011.10.046 22192827

14. Macosko EZ, Pokala N, Feinberg EH, Chalasani SH, Butcher RA, et al. (2009) A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458: 1171–1175. doi: 10.1038/nature07886 19349961

15. Gray JM, Karow DS, Lu H, Chang AJ, Chang JS, et al. (2004) Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430: 317–322. 15220933

16. Cheung BH, Cohen M, Rogers C, Albayram O, de Bono M (2005) Experience-dependent modulation of C. elegans behavior by ambient oxygen. Current biology: CB 15: 905–917. 15916947

17. Coates JC, de Bono M (2002) Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans. Nature 419: 925–929. 12410311

18. de Bono M, Tobin DM, Davis MW, Avery L, Bargmann CI (2002) Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli. Nature 419: 899–903. 12410303

19. Nagy S, Raizen DM, Biron D (2014) Measurements of behavioral quiescence in Caenorhabditis elegans. Methods 68: 500–507. doi: 10.1016/j.ymeth.2014.03.009 24642199

20. Nagy S, Tramm N, Sanders J, Iwanir S, Shirley IA, et al. (2014) Homeostasis in C. elegans sleep is characterized by two behaviorally and genetically distinct mechanisms. Elife 3: e04380. doi: 10.7554/eLife.04380 25474127

21. de Bono M, Bargmann CI (1998) Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94: 679–689. 9741632

22. Vashlishan AB, Madison JM, Dybbs M, Bai J, Sieburth D, et al. (2008) An RNAi screen identifies genes that regulate GABA synapses. Neuron 58: 346–361. doi: 10.1016/j.neuron.2008.02.019 18466746

23. Lee RY, Sawin ER, Chalfie M, Horvitz HR, Avery L (1999) EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in caenorhabditis elegans. The Journal of neuroscience: the official journal of the Society for Neuroscience 19: 159–167.

24. Tobin D, Madsen D, Kahn-Kirby A, Peckol E, Moulder G, et al. (2002) Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35: 307–318. 12160748

25. Brockie PJ, Madsen DM, Zheng Y, Mellem J, Maricq AV (2001) Differential expression of glutamate receptor subunits in the nervous system of Caenorhabditis elegans and their regulation by the homeodomain protein UNC-42. The Journal of neuroscience: the official journal of the Society for Neuroscience 21: 1510–1522.

26. Hart AC, Sims S, Kaplan JM (1995) Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378: 82–85. 7477294

27. Maricq AV, Peckol E, Driscoll M, Bargmann CI (1995) Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature 378: 78–81. 7477293

28. White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of Caenorhabditis elegans. Philos Trans R Soc Lond 314: 1–340.

29. Janssen T, Husson SJ, Meelkop E, Temmerman L, Lindemans M, et al. (2009) Discovery and characterization of a conserved pigment dispersing factor-like neuropeptide pathway in Caenorhabditis elegans. Journal of neurochemistry 111: 228–241. doi: 10.1111/j.1471-4159.2009.06323.x 19686386

30. Fares H, Greenwald I (2001) Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants. Genetics 159: 133–145. 11560892

31. Sieburth D, Madison JM, Kaplan JM (2007) PKC-1 regulates secretion of neuropeptides. Nature neuroscience 10: 49–57. 17128266

32. White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical transactions of the Royal Society of London Series B, Biological sciences 314: 1–340. 22462104

33. Hu Z, Pym EC, Babu K, Vashlishan Murray AB, Kaplan JM (2011) A neuropeptide-mediated stretch response links muscle contraction to changes in neurotransmitter release. Neuron 71: 92–102. doi: 10.1016/j.neuron.2011.04.021 21745640

34. Parisky KM, Agosto J, Pulver SR, Shang Y, Kuklin E, et al. (2008) PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit. Neuron 60: 672–682. doi: 10.1016/j.neuron.2008.10.042 19038223

35. Prober DA, Rihel J, Onah AA, Sung RJ, Schier AF (2006) Hypocretin/orexin overexpression induces an insomnia-like phenotype in zebrafish. J Neurosci 26: 13400–13410. 17182791

36. Sutcliffe JG, de Lecea L (2002) The hypocretins: setting the arousal threshold. Nature reviews Neuroscience 3: 339–349. 11988773

37. Alam MA, Mallick BN (2008) Glutamic acid stimulation of the perifornical-lateral hypothalamic area promotes arousal and inhibits non-REM/REM sleep. Neurosci Lett 439: 281–286. doi: 10.1016/j.neulet.2008.05.042 18534750

38. Li FW, Deurveilher S, Semba K (2011) Behavioural and neuronal activation after microinjections of AMPA and NMDA into the perifornical lateral hypothalamus in rats. Behav Brain Res 224: 376–386. doi: 10.1016/j.bbr.2011.06.021 21723327

39. Juhasz G, Kekesi K, Emri Z, Soltesz I, Crunelli V (1990) Sleep-promoting action of excitatory amino acid antagonists: a different role for thalamic NMDA and non-NMDA receptors. Neurosci Lett 114: 333–338. 1976237

40. Brodin L, Grillner S, Rovainen CM (1985) N-Methyl-D-aspartate (NMDA), kainate and quisqualate receptors and the generation of fictive locomotion in the lamprey spinal cord. Brain Res 325: 302–306. 2858251

41. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94. 4366476

42. Nurrish S, Segalat L, Kaplan JM (1999) Serotonin inhibition of synaptic transmission: Galpha(0) decreases the abundance of UNC-13 at release sites. Neuron 24: 231–242. 10677040

43. Richmond JE, Davis WS, Jorgensen EM (1999) UNC-13 is required for synaptic vesicle fusion in C. elegans. Nature neuroscience 2: 959–964. 10526333

44. McEwen JM, Madison JM, Dybbs M, Kaplan JM (2006) Antagonistic regulation of synaptic vesicle priming by Tomosyn and UNC-13. Neuron 51: 303–315. 16880125

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