Sleep-active neuron specification and sleep induction require FLP-11 neuropeptides to systemically induce sleep

eLife

Volumn 5, Issue MARCH2016, 2016, Pages

  Turek, Michal ^a   Besseling, Judith ^a   Spies, Jan Philipp ^a   König, Sabine ^a   Bringmann, Henrik ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; FLP 11 SLEEP INDUCING PEPTIDE; G PROTEIN COUPLED RECEPTOR; HEAT SHOCK PROTEIN; LIM 6 PROTEIN; LIM PROTEIN; NEUROPEPTIDE; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; CAENORHABDITIS ELEGANS PROTEIN; LIM HOMEODOMAIN PROTEIN; LIM-6 PROTEIN, C ELEGANS; THIOL ESTER HYDROLASE; TRANSCRIPTION FACTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAENORHABDITIS ELEGANS; EMBRYO; FLUORESCENCE IMAGING; GENE EXPRESSION; GENE EXPRESSION PROFILING; MOLECULAR BIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTOGENETICS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SLEEP INDUCTION; SLEEP WAKING CYCLE; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; ANIMAL; METABOLISM; PHYSIOLOGY; SLEEP;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GABAERGIC NEURONS; LIM-HOMEODOMAIN PROTEINS; NEUROPEPTIDES; SLEEP; THIOLESTER HYDROLASES; TRANSCRIPTION FACTORS;

EID: 84964296807     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.12499     Document Type: Article

References (94)

1. Alam MA, Kumar S, McGinty D, Alam MN, Szymusiak R. 2014. Neuronal activity in the preoptic hypothalamus during sleep deprivation and recovery sleep. Journal of Neurophysiology 111:287–299. doi: 10.1152/jn.00504.2013
2. Anaclet C, Ferrari L, Arrigoni E, Bass CE, Saper CB, Lu J, Fuller PM. 2014. The GABAergic parafacial zone is a medullary slow wave sleep-promoting center. Nature Neuroscience 17:1217–1224. doi: 10.1038/nn.3789
3. Anaclet C, Lin JS, Vetrivelan R, Krenzer M, Vong L, Fuller PM, Lu J. 2012. Identification and characterization of a sleep-active cell group in the rostral medullary brainstem. Journal of Neuroscience 32:17970–17976. doi: 10.1523/JNEUROSCI.0620-12.2012
4. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71–94.
5. Bringmann H. 2011. Agarose hydrogel microcompartments for imaging sleep-and wake-like behavior and nervous system development in Caenorhabditis elegans larvae. Journal of Neuroscience Methods 201:78–88. doi: 10.1016/j.jneumeth.2011.07.013
6. Butler VJ. 2012. Molecular and Neuromuscular Mechanisms Underlying Locomotion and Proprioception in Caenorhabditis Elegans. Dissertation, MRC Laboratory of Molecular Biology, Downing College, University of Cambridge.
7. Campbell SS, Tobler I. 1984. Animal sleep: a review of sleep duration across phylogeny. Neuroscience and Biobehavioral Reviews 8:269–300. doi: 10.1016/0149-7634(84)90054-X
8. Cassada RC, Russell RL. 1975. The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Developmental Biology 46:326–342. doi: 10.1016/0012-1606(75)90109-8
9. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. 1994. Green fluorescent protein as a marker for gene expression. Science 263:802–805. doi: 10.1126/science.8303295
10. Chen W, Shi W, Li L, Zheng Z, Li T, Bai W, Zhao Z. 2013. Regulation of sleep by the short neuropeptide F (sNPF) in Drosophila melanogaster. Insect Biochemistry and Molecular Biology 43:809–819. doi: 10.1016/j.ibmb.2013.06.003
11. 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
12. 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
13. Cirelli C, Tononi G. 2008. Is sleep essential? PLoS Biology 6:e216. doi: 10.1371/journal.pbio.0060216
14. Cohen M, Reale V, Olofsson B, Knights A, Evans P, de Bono M. 2009. Coordinated regulation of foraging and metabolism in C. elegans by RFamide neuropeptide signaling. Cell Metabolism 9:375–385. doi: 10.1016/j.cmet.2009.02.003
15. Dabbish NS, Raizen DM. 2011. GABAergic synaptic plasticity during a developmentally regulated sleep-like state in C. elegans. Journal of Neuroscience 31:15932–15943. doi: 10.1523/JNEUROSCI.0742-11.2011
16. Donnelly JL, Clark CM, Leifer AM, Pirri JK, Haburcak M, Francis MM, Samuel AD, Alkema MJ. 2013. Monoaminergic orchestration of motor programs in a complex C. elegans behavior. PLoS Biology 11: e1001529. doi: 10.1371/journal.pbio.1001529
17. Driver RJ, Lamb AL, Wyner AJ, Raizen DM. 2013. DAF-16/FOXO regulates homeostasis of essential sleep-like behavior during larval transitions in C. elegans. Current Biology: CB 23:501–506. doi: 10.1016/j.cub.2013.02.009
18. Eckert D, Buhl S, Weber S, Jäger R, Schorle H. 2005. The AP-2 family of transcription factors. Genome Biology 6: 246. doi: 10.1186/gb-2005-6-13-246
19. Friedland AE, Tzur YB, Esvelt KM, Colaiácovo MP, Church GM, Calarco JA. 2013. Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nature Methods 10:741–743. doi: 10.1038/nmeth.2532
20. Frooninckx L, Van Rompay L, Temmerman L, Van Sinay E, Beets I, Janssen T, Husson SJ, Schoofs L. 2012. Neuropeptide GPCRs in C. elegans. Frontiers in Endocrinology 3:167. doi: 10.3389/fendo.2012.00167
21. Gallopin T, Fort P, Eggermann E, Cauli B, Luppi PH, Rossier J, Audinat E, Mühlethaler M, Serafin M. 2000. Identification of sleep-promoting neurons in vitro. Nature 404:992–995. doi: 10.1038/35010109
22. Gaus SE, Strecker RE, Tate BA, Parker RA, Saper CB. 2002. Ventrolateral preoptic nucleus contains sleep-active, galaninergic neurons in multiple mammalian species. Neuroscience 115:285–294. doi: 10.1016/S0306-4522(02)00308-1
23. Grant CE, Bailey TL, Noble WS. 2011. FIMO: scanning for occurrences of a given motif. Bioinformatics 27:1017–1018. doi: 10.1093/bioinformatics/btr064
24. Halder G, Callaerts P, Gehring WJ. 1995. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267:1788–1792. doi: 10.1126/science.7892602
25. Hill AJ, Mansfield R, Lopez JM, Raizen DM, Van Buskirk C. 2014. Cellular stress induces a protective sleep-like state in C. elegans. Current Biology 24:2399–2405. doi: 10.1016/j.cub.2014.08.040
26. Hobert O, Tessmar K, Ruvkun G. 1999. The Caenorhabditis elegans lim-6 LIM homeobox gene regulates neurite outgrowth and function of particular GABAergic neurons. Development 126:1547–1562.
27. Iwanir S, Tramm N, Nagy S, Wright C, Ish D, Biron D. 2013. The microarchitecture of C. elegans behavior during lethargus: homeostatic bout dynamics, a typical body posture, and regulation by a central neuron. Sleep 36: 385–395. doi: 10.5665/sleep.2456
28. Jeon M, Gardner HF, Miller EA, Deshler J, Rougvie AE. 1999. Similarity of the C. elegans developmental timing protein LIN-42 to circadian rhythm proteins. Science 286:1141–1146. doi: 10.1126/science.286.5442.1141
29. Jin Y, Jorgensen E, Hartwieg E, Horvitz HR. 1999. The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. The Journal of Neuroscience 19:539–548.
30. Jones D, Russnak RH, Kay RJ, Candido EP. 1986. Structure, expression, and evolution of a heat shock gene locus in Caenorhabditis elegans that is flanked by repetitive elements. The Journal of Biological Chemistry 261: 12006–12015.
31. Kerr BJ, Cafferty WB, Gupta YK, Bacon A, Wynick D, McMahon SB, Thompson SW. 2000. Galanin knockout mice reveal nociceptive deficits following peripheral nerve injury. The European Journal of Neuroscience 12:793–802. doi: 10.1046/j.1460-9568.2000.00967.x
32. Kim K, Li C. 2004. Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. The Journal of Comparative Neurology 475:540–550. doi: 10.1002/cne.20189
33. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology 305:567–580. doi: 10.1006/jmbi.2000.4315
34. Lang R, Gundlach AL, Kofler B. 2007. The galanin peptide family: receptor pharmacology, pleiotropic biological actions, and implications in health and disease. Pharmacology & Therapeutics 115:177–207. doi: 10.1016/j.pharmthera.2007.05.009
35. Li C, Nelson LS, Kim K, Nathoo A, Hart AC. 1999. Neuropeptide gene families in the nematode Caenorhabditis elegans. Annals of the New York Academy of Sciences 897:239–252. doi: 10.1111/j.1749-6632.1999.tb07895.x
36. Mani A, Radhakrishnan J, Farhi A, Carew KS, Warnes CA, Nelson-Williams C, Day RW, Pober B, State MW, Lifton RP. 2005. Syndromic patent ductus arteriosus: Evidence for haploinsufficient TFAP2B mutations and identification of a linked sleep disorder. Proceedings of the National Academy of Sciences of the United States of America 102:2975–2979. doi: 10.1073/pnas.0409852102
37. McGinty D, Gong H, Suntsova N, Alam MN, Methippara M, Guzman-Marin R, Szymusiak R. 2004. Sleep-promoting functions of the hypothalamic median preoptic nucleus: inhibition of arousal systems. Archives Italiennes De Biologie 142:501–509.
38. McGinty DJ, Sterman MB. 1968. Sleep suppression after basal forebrain lesions in the cat. Science 160:1253–1255. doi: 10.1126/science.160.3833.1253
39. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM. 1997. Identification and characterization of the vesicular GABA transporter. Nature 389:870–876. doi: 10.1038/39908
40. Merritt C, Seydoux G. 2010. Transgenic solutions for the germline. WormBook: The Online Review of C. Elegans Biology:1–21. doi: 10.1895/wormbook.1.148.1
41. Mertens I, Clinckspoor I, Janssen T, Nachman R, Schoofs L. 2006. FMRFamide related peptide ligands activate the Caenorhabditis elegans orphan GPCR Y59H11AL.1. Peptides 27:1291–1296. doi: 10.1016/j.peptides.2005.11.017
42. Mertens I, Vandingenen A, Meeusen T, Janssen T, Luyten W, Nachman RJ, De Loof A, Schoofs L. 2004. Functional characterization of the putative orphan neuropeptide G-protein coupled receptor C26F1.6 in Caenorhabditis elegans. FEBS Letters 573:55–60. doi: 10.1016/j.febslet.2004.07.058
43. Monsalve GC, Van Buskirk C, Frand AR. 2011. LIN-42/PERIOD controls cyclical and developmental progression of C. elegans molts. Current Biology 21:2033–2045. doi: 10.1016/j.cub.2011.10.054
44. Moruzzi G, Magoun HW. 1949. Brain stem reticular formation and activation of the EEG. Electroencephalography and Clinical Neurophysiology 1:455–473. doi: 10.1016/0013-4694(49)90219-9
45. Murck H, Held K, Ziegenbein M, Künzel H, Holsboer F, Steiger A. 2004. Intravenous administration of the neuropeptide galanin has fast antidepressant efficacy and affects the sleep EEG. Psychoneuroendocrinology 29:1205–1211. doi: 10.1016/j.psyneuen.2004.02.006
46. Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A. 2005. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Current Biology 15:2279–2284. doi: 10.1016/j.cub.2005.11.032
47. Nagy S, Tramm N, Sanders J, Iwanir S, Shirley IA, Levine E, Biron D. 2014. Homeostasis in C. elegans sleep is characterized by two behaviorally and genetically distinct mechanisms. eLife 3:e04380. doi: 10.7554/eLife.04380
48. Nass R, Hall DH, Miller DM, Blakely RD. 2002. Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 99: 3264–3269. doi: 10.1073/pnas.042497999
49. Nauta WJ. 1946. Hypothalamic regulation of sleep in rats; an experimental study. Journal of Neurophysiology 9: 285–316.
50. Nelson MD, Lee KH, Churgin MA, Hill AJ, Van Buskirk C, Fang-Yen C, Raizen DM. 2014. FMRFamide-like FLP-13 neuropeptides promote quiescence following heat stress in Caenorhabditis elegans. Current Biology 24:2406–2410. doi: 10.1016/j.cub.2014.08.037
51. Nelson MD, Trojanowski NF, George-Raizen JB, Smith CJ, Yu CC, Fang-Yen C, Raizen DM. 2013. The neuropeptide NLP-22 regulates a sleep-like state in Caenorhabditis elegans. Nature Communications 4:2846. doi: 10.1038/ncomms3846
52. Ni K-M, Hou X-J, Yang C-H, Dong P, Li Y, Zhang Y, Jiang P, Berg DK, Duan S, Li X-M. 2016. Selectively driving cholinergic fibers optically in the thalamic reticular nucleus promotes sleep. eLife 5. doi: 10.7554/eLife.10382
53. Nitta KR, Jolma A, Yin Y, Morgunova E, Kivioja T, Akhtar J, Hens K, Toivonen J, Deplancke B, Furlong EE, Taipale J. 2015. Conservation of transcription factor binding specificities across 600 million years of bilateria evolution. eLife 4. doi: 10.7554/eLife.04837
54. Panossian LA, Avidan AY. 2009. Review of sleep disorders. The Medical Clinics of North America 93:407–425. doi: 10.1016/j.mcna.2008.09.001
55. Peymen K, Watteyne J, Frooninckx L, Schoofs L, Beets I. 2014. The FMRFamide-Like Peptide Family in Nematodes. Frontiers in Endocrinology 5:90. doi: 10.3389/fendo.2014.00090
56. Pieribone VA, Xu ZQ, Zhang X, Grillner S, Bartfai T, Hökfelt T. 1995. Galanin induces a hyperpolarization of norepinephrine-containing locus coeruleus neurons in the brainstem slice. Neuroscience 64:861–874. doi: 10.1016/0306-4522(94)00450-J
57. Praitis V, Casey E, Collar D, Austin J. 2001. Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157:1217–1226.
58. Raizen DM, Zimmerman JE, Maycock MH, Ta UD, You YJ, Sundaram MV, Pack AI. 2008. Lethargus is a Caenorhabditis elegans sleep-like state. Nature 451:569–572. doi: 10.1038/nature06535
59. Rechtschaffen A, Bergmann BM. 1995. Sleep deprivation in the rat by the disk-over-water method. Behavioural Brain Research 69:55–63. doi: 10.1016/0166-4328(95)00020-T
60. Redemann S, Schloissnig S, Ernst S, Pozniakowsky A, Ayloo S, Hyman AA, Bringmann H. 2011. Codon adaptation-based control of protein expression in C. elegans. Nature Methods 8:250–252. doi: 10.1038/nmeth.1565
61. Saper CB, Chou TC, Scammell TE. 2001. The sleep switch: hypothalamic control of sleep and wakefulness. Trends in Neurosciences 24:726–731. doi: 10.1016/S0166-2236(00)02002-6
62. Saper CB, Scammell TE, Lu J. 2005. Hypothalamic regulation of sleep and circadian rhythms. Nature 437:1257–1263. doi: 10.1038/nature04284
63. Sarov M, Murray JI, Schanze K, Pozniakovski A, Niu W, Angermann K, Hasse S, Rupprecht M, Vinis E, Tinney M, Preston E, Zinke A, Enst S, Teichgraber T, Janette J, Reis K, Janosch S, Schloissnig S, Ejsmont RK, Slightam C, Xu X, Kim SK, Reinke V, Stewart AF, Snyder M, Waterston RH, Hyman AA. 2012. A genome-scale resource for in vivo tag-based protein function exploration in C. elegans. Cell 150:855–866. doi: 10.1016/j.cell.2012.08.001
64. Schwarz J, Bringmann H. 2013. Reduced sleep-like quiescence in both hyperactive and hypoactive mutants of the Galphaq Gene egl-30 during lethargus in Caenorhabditis elegans. PloS One 8:e75853. doi: 10.1371/journal.pone.0075853
65. Schwarz J, Lewandrowski I, Bringmann H. 2011. Reduced activity of a sensory neuron during a sleep-like state in Caenorhabditis elegans. Current Biology 21:R983–R984. doi: 10.1016/j.cub.2011.10.046
66. Schwarz J, Spies JP, Bringmann H. 2012. Reduced muscle contraction and a relaxed posture during sleep-like Lethargus. Worm 1:12–14. doi: 10.4161/worm.19499
67. Seutin V, Verbanck P, Massotte L, Dresse A. 1989. Galanin decreases the activity of locus coeruleus neurons in vitro. European Journal of Pharmacology 164:373–376. doi: 10.1016/0014-2999(89)90481-0
68. Shang Y, Donelson NC, Vecsey CG, Guo F, Rosbash M, Griffith LC. 2013. Short neuropeptide F is a sleep-promoting inhibitory modulator. Neuron 80:171–183. doi: 10.1016/j.neuron.2013.07.029
69. Shcherbo D, Murphy CS, Ermakova GV, Solovieva EA, Chepurnykh TV, Shcheglov AS, Verkhusha VV, Pletnev VZ, Hazelwood KL, Roche PM, Lukyanov S, Zaraisky AG, Davidson MW, Chudakov DM. 2009. Far-red fluorescent tags for protein imaging in living tissues. The Biochemical Journal 418:567–574. doi: 10.1042/BJ20081949
70. Sherin JE, Elmquist JK, Torrealba F, Saper CB. 1998. Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. The Journal of Neuroscience 18:4705–4721.
71. Sherin JE, Shiromani PJ, McCarley RW, Saper CB. 1996. Activation of ventrolateral preoptic neurons during sleep. Science 271:216–219. doi: 10.1126/science.271.5246.216
72. Singh K, Chao MY, Somers GA, Komatsu H, Corkins ME, Larkins-Ford J, Tucey T, Dionne HM, Walsh MB, Beaumont EK, Hart DP, Lockery SR, Hart AC. 2011. C. elegans Notch signaling regulates adult chemosensory response and larval molting quiescence. Current Biology 21:825–834. doi: 10.1016/j.cub.2011.04.010
73. Singh K, Ju JY, Walsh MB, DiIorio MA, Hart AC. 2014. Deep conservation of genes required for both Drosphila melanogaster and Caenorhabditis elegans sleep includes a role for dopaminergic signaling. Sleep 37. doi: 10.5665/sleep.3990
74. Starzl TE, Taylor CW, Magoun HW. 1951. Ascending conduction in reticular activating system, with special reference to the diencephalon. Journal of Neurophysiology 14:461–477.
75. Szymusiak R, Alam N, Steininger TL, McGinty D. 1998. Sleep-waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats. Brain Research 803:178–188. doi: 10.1016/S0006-8993(98)00631-3
76. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL. 2009. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nature Methods 6:875–881. doi: 10.1038/nmeth.1398
77. Trojanowski NF, Nelson MD, Flavell SW, Fang-Yen C, Raizen DM. 2015. Distinct Mechanisms Underlie Quiescence during Two Caenorhabditis elegans Sleep-Like States. Journal of Neuroscience 35:14571–14584. doi: 10.1523/JNEUROSCI.1369-15.2015
78. Trojanowski NF, Raizen DM. 2016. Call it Worm Sleep. Trends in Neurosciences 39:54–62. doi: 10.1016/j.tins.2015.12.005
79. Tsalik EL, Niacaris T, Wenick AS, Pau K, Avery L, Hobert O. 2003. LIM homeobox gene-dependent expression of biogenic amine receptors in restricted regions of the C. elegans nervous system. Developmental Biology 263: 81–102. doi: 10.1016/S0012-1606(03)00447-0
80. Turek M, Besseling J, Bringmann H. 2015.;in press Agarose Microchambers for Long-term Calcium Imaging of Caenorhabditis elegans. Journal of Visualized Experiments. doi: 10.3791/52742
81. Turek M, Bringmann H. 2014. Gene expression changes of Caenorhabditis elegans larvae during molting and sleep-like lethargus. PloS One 9:e113269. doi: 10.1371/journal.pone.0113269
82. 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. Current Biology 23:2215–2223. doi: 10.1016/j.cub.2013.09.028
83. Van Buskirk C, Sternberg PW. 2007. Epidermal growth factor signaling induces behavioral quiescence in Caenorhabditis elegans. Nature Neuroscience 10:1300–1307. doi: 10.1038/nn1981
84. Vecsey CG, Pírez N, Griffith LC. 2014. The Drosophila neuropeptides PDF and sNPF have opposing electrophysiological and molecular effects on central neurons. Journal of Neurophysiology 111:1033–1045. doi: 10.1152/jn.00712.2013
85. von Economo V. 1930. Sleep as a problem of localization. The Journal of Nervous and Mental Disease 71:249–259. doi: 10.1097/00005053-193003000-00001
86. Vrontakis ME. 2002. Galanin: A Biologically Active Peptide. Current Drug Target-CNS & Neurological Disorders 1:531–541. doi: 10.2174/1568007023338914
87. 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 B: Biological Sciences 314:1–340. doi: 10.1098/rstb.1986.0056
88. Wightman B, Ebert B, Carmean N, Weber K, Clever S. 2005. The C. elegans nuclear receptor gene fax-1 and homeobox gene unc-42 coordinate interneuron identity by regulating the expression of glutamate receptor subunits and other neuron-specific genes. Developmental Biology 287:74–85. doi: 10.1016/j.ydbio.2005.08.032
89. Wilm T, Demel P, Koop HU, Schnabel H, Schnabel R. 1999. Ballistic transformation of Caenorhabditis elegans. Gene 229:31–35. doi: 10.1016/S0378-1119(99)00043-8
90. Woods IG, Schoppik D, Shi VJ, Zimmerman S, Coleman HA, Greenwood J, Soucy ER, Schier AF. 2014. Neuropeptidergic signaling partitions arousal behaviors in zebrafish. Journal of Neuroscience 34:3142–3160. doi: 10.1523/JNEUROSCI.3529-13.2014
91. Wynick D, Small CJ, Bacon A, Holmes FE, Norman M, Ormandy CJ, Kilic E, Kerr NCH, Ghatei M, Talamantes F, Bloom SR, Pachnis V. 1998. Galanin regulates prolactin release and lactotroph proliferation. Proceedings of the National Academy of Sciences of the United States of America 95:12671–12676. doi: 10.1073/pnas.95.21.12671
92. Yew JY, Davis R, Dikler S, Nanda J, Reinders B, Stretton AO. 2007. Peptide products of the afp-6 gene of the nematode Ascaris suum have different biological actions. The Journal of Comparative Neurology 502:872–882. doi: 10.1002/cne.21357
93. You YJ, Kim J, Raizen DM, Avery L. 2008. Insulin, cGMP, and TGF-beta signals regulate food intake and quiescence in C. elegans: a model for satiety. Cell Metabolism 7:249–257. doi: 10.1016/j.cmet.2008.01.005
94. Zhao F, Bosserhoff AK, Buettner R, Moser M. 2011. A heart-hand syndrome gene: Tfap2b plays a critical role in the development and remodeling of mouse ductus arteriosus and limb patterning. PloS One 6:e22908. doi: 10.1371/journal.pone.0022908