Genetic ablation of hypocretin neurons alters behavioral state transitions in zebrafish

Journal of Neuroscience

Volumn 32, Issue 37, 2012, Pages 12961-12972

  Elbaz, Idan ^a   Yelin Bekerman, Laura ^a   Nicenboim, Julian ^b   Vatine, Gad ^a   Appelbaum, Lior ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; METRONIDAZOLE; NITROREDUCTASE; OREXIN; OREXIN 1 RECEPTOR; OREXIN 2 RECEPTOR; PROTEIN C FOS;

ABLATION THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; BEHAVIOR; BRAIN NERVE CELL; CELL LOSS; CONTROLLED STUDY; EMBRYO; FEMALE; LARVA; LIGHT DARK CYCLE; LOCOMOTION; MALE; NARCOLEPSY; NERVE ABLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SLEEP AROUSAL DISORDER; SLEEP TIME; SLEEP WAKING CYCLE; VISUAL STIMULATION; ZEBRA FISH;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; GENE SILENCING; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LOCOMOTION; NARCOLEPSY; NEURONS; NEUROPEPTIDES; SLEEP STAGES; ZEBRAFISH;

EID: 84866241638     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1284-12.2012     Document Type: Article

References (55)

1. Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L (2007) Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 450:420-424.
2. Appelbaum L, Wang GX, Maro GS, Mori R, Tovin A, Marin W, Yokogawa T, Kawakami K, Smith SJ, Gothilf Y, Mignot E, Mourrain P (2009) Sleepwake regulation and hypocretin-melatonin interaction in zebrafish. Proc Natl Acad Sci U S A 106:21942-21947.
3. Appelbaum L, Wang G, Yokogawa T, Skariah GM, Smith SJ, Mourrain P, Mignot E (2010) Circadian and homeostatic regulation of structural synaptic plasticity in hypocretin neurons. Neuron 68:87-98.
4. Berman JR, Skariah G, Maro GS, Mignot E, Mourrain P (2009) Characterization of two melanin-concentrating hormone genes in zebrafish reveals evolutionary and physiological links with the mammalian MCH system. J Comp Neurol 517:695-710.
5. Bonnavion P, de Lecea L (2010) Hypocretins in the control of sleep and wakefulness. Curr Neurol Neurosci Rep 10:174-179.
6. Cahill GM, Hurd MW, Batchelor MM (1998) Circadian rhythmicity in the locomotor activity of larval zebrafish. Neuroreport 9:3445-3449.
7. Carter ME, Adamantidis A, Ohtsu H, Deisseroth K, de Lecea L (2009) Sleep homeostasis modulates hypocretin-mediated sleep-to-wake transitions. J Neurosci 29:10939-10949.
8. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C, Richardson JA, Williams SC, Xiong Y, Kisanuki Y, Fitch TE, Nakazato M, Hammer RE, Saper CB, Yanagisawa M (1999) Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98:437-451.
9. Cirelli C, Tononi G (2000) On the functional significance of c-fos induction during the sleep-waking cycle. Sleep 23:453-469.
10. Colwill RM, Creton R (2011) Imaging escape and avoidance behavior in zebrafish larvae. Rev Neurosci 22:63-73.
11. Curado S, Stainier DY, Anderson RM (2008) Nitroreductase-mediated cell/ tissue ablation in zebrafish: a spatially and temporally controlled ablation method with applications in developmental and regeneration studies. Nat Protoc 3:948-954.
12. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, Fukuhara C, Battenberg EL, Gautvik VT, Bartlett FS 2nd, Frankel WN, van den Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG (1998) The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A 95:322-327.
13. Emran F, Rihel J, Dowling JE (2008) A behavioral assay to measure responsiveness of zebrafish to changes in light intensities. J Vis Exp 2008:pii: 923.
14. Faraco JH, Appelbaum L, Marin W, Gaus SE, Mourrain P, Mignot E (2006) Regulation of hypocretin (orexin) expression in embryonic zebrafish. J Biol Chem 281:29753-29761.
15. Furlong TM, Vianna DM, Liu L, Carrive P (2009) Hypocretin/orexin contributes to the expression of some but not all forms of stress and arousal. Eur J Neurosci 30:1603-1614.
16. Hara J, Beuckmann CT, Nambu T, Willie JT, Chemelli RM, Sinton CM, Sugiyama F, Yagami K, Goto K, Yanagisawa M, Sakurai T (2001) Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron 30:345-354.
17. Hara J, Yanagisawa M, Sakurai T (2005) Difference in obesity phenotype between orexin-knockout mice and orexin neuron-deficient mice with same genetic background and environmental conditions. Neurosci Lett 380:239-242.
18. Hendricks JC, Sehgal A, Pack AI (2000) The need for a simple animal model to understand sleep. Prog Neurobiol 61:339-351.
19. Kaslin J, Nystedt JM, Ostergård M, Peitsaro N, Panula P (2004) The orexin/ hypocretin system in zebrafish is connected to the aminergic and cholinergic systems. J Neurosci 24:2678-2689.
20. Kawakami K (2004) Transgenesis and gene trap methods in zebrafish by using the Tol2 transposable element. In: Methods in cell biology (Detrich HW III, Westerfield M, Zon LI, eds), pp 201-222. Waltham, MA: Academic.
21. Kayaba Y, Nakamura A, Kasuya Y, Ohuchi T, Yanagisawa M, Komuro I, Fukuda Y, Kuwaki T (2003) Attenuated defense response and low basal blood pressure in orexin knockout mice. Am J Physiol Regul Integr Comp Physiol 285:R581-R593.
22. Lin L, Faraco J, Li R, Kadotani H, Rogers W, Lin X, Qiu X, de Jong PJ, Nishino S, Mignot E (1999) The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 98:365-376.
23. Matsuki T, Nomiyama M, Takahira H, Hirashima N, Kunita S, Takahashi S, Yagami K, Kilduff TS, Bettler B, Yanagisawa M, Sakurai T (2009) Selective loss of GABA(B) receptors in orexin-producing neurons results in disrupted sleep/wakefulness architecture. Proc Natl Acad Sci U S A 106:4459-4464.
24. Mieda M, Willie JT, Hara J, Sinton CM, Sakurai T, Yanagisawa M (2004) Orexin peptides prevent cataplexy and improve wakefulness in an orexin neuron-ablated model of narcolepsy in mice. Proc Natl Acad Sci U S A 101:4649-4654.
25. Montgomery JE, Parsons MJ, Hyde DR (2010) A novel model of retinal ablation demonstrates that the extent of rod cell death regulates the origin of the regenerated zebrafish rod photoreceptors. J Comp Neurol 518:800-814.
26. Naumann EA, Kampff AR, Prober DA, Schier AF, Engert F (2010) Monitoring neural activity with bioluminescence during natural behavior. Nat Neurosci 13:513-520.
27. Nishino S, Mignot E (1997) Pharmacological aspects of human and canine narcolepsy. Prog Neurobiol 52:27-78.
28. Nishino S, Sakurai T (2006) The orexin/hypocretin system: physiology and pathophysiology. Towota, NJ: Humana.
29. Nishino S, Fujiki N, Ripley B, Sakurai E, Kato M, Watanabe T, Mignot E, Yanai K (2001) Decreased brain histamine content in hypocretin/orexin receptor-2 mutated narcoleptic dogs. Neurosci Lett 313:125-128.
30. Panula P (2010) Hypocretin/orexin in fish physiology with emphasis on zebrafish. Acta Physiol (Oxf) 198:381-386.
31. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, Kilduff TS (1998) Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18:9996-10015.
32. Peyron C, Faraco J, Rogers W, Ripley B, Overeem S, Charnay Y, Nevsimalova S, Aldrich M, Reynolds D, Albin R, Li R, Hungs M, Pedrazzoli M, Padigaru M, Kucherlapati M, Fan J, Maki R, Lammers GJ, Bouras C, Kucherlapati R, Nishino S, Mignot E (2000) A mutation in a case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat Med 6:991-997.
33. Pisharath H, Parsons MJ (2009) Nitroreductase-mediated cell ablation in transgenic zebrafish embryos. Methods Mol Biol 546:133-143.
34. Pisharath H, Rhee JM, Swanson MA, Leach SD, Parsons MJ (2007) Targeted ablation of beta cells in the embryonic zebrafish pancreas using E. coli nitroreductase. Mech Dev 124:218-229.
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.
36. 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.
37. Rihel J, Prober DA, Schier AF (2010) Monitoring sleep and arousal in zebrafish. Methods Cell Biol 100:281-294.
38. Sakurai T (2007) The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 8:171-181.
39. Sakurai T, Mieda M (2011) Connectomics of orexin-producing neurons: interface of systems of emotion, energy homeostasis and arousal. Trends Pharmacol Sci 32:451-462.
40. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richarson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G proteincoupled receptors that regulate feeding behavior. Cell 92: 696.
41. Saper CB, Scammell TE, Lu J (2005) Hypothalamic regulation of sleep and circadian rhythms. Nature 437:1257-1263.
42. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108.
43. Sehgal A, Mignot E (2011) Genetics of sleep and sleep disorders. Cell 146:194-207.
44. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834-1837.
45. Siegel JM (2005) Clues to the functions of mammalian sleep. Nature 437:1264-1271.
46. Sigurgeirsson B, Thornorsteinsson H, Arnardóttir H, Jóhannesdottir IT, Karlsson KA (2011) Effects of modafinil on sleep-wake cycles in larval zebrafish. Zebrafish 8:133-140.
47. Van Epps HA, Yim CM, Hurley JB, Brockerhoff SE (2001) Investigations of photoreceptor synaptic transmission and light adaptation in the zebrafish visual mutant nrc. Invest Ophthalmol Vis Sci 42:868-874.
48. Willie JT, Chemelli RM, Sinton CM, Tokita S, Williams SC, Kisanuki YY, Marcus JN, Lee C, Elmquist JK, Kohlmeier KA, Leonard CS, Richardson JA, Hammer RE, Yanagisawa M (2003) Distinct narcolepsy syndromes in orexin receptor-2 and orexin null mice: molecular genetic dissection of non-REM and REM sleep regulatory processes. Neuron 38:715-730.
49. Winsky-Sommerer R, Yamanaka A, Diano S, Borok E, Roberts AJ, Sakurai T, Kilduff TS, Horvath TL, de Lecea L (2004) Interaction between the corticotropin-releasing factor system and hypocretins (orexins): a novel circuit mediating stress response. J Neurosci 24:11439-11448.
50. Yokogawa T, Marin W, Faraco J, Pézeron G, Appelbaum L, Zhang J, Rosa F, Mourrain P, Mignot E (2007) Characterization of sleep in zebrafish and insomnia in hypocretin receptor mutants. PLo S Biol 5:e277.
51. Zhang W, Zhang N, Sakurai T, Kuwaki T (2009) Orexin neurons in the hypothalamus mediate cardiorespiratory responses induced by disinhibition of the amygdala and bed nucleus of the stria terminalis. Brain Res 1262:25-37.
52. Zhao XF, Ellingsen S, Fjose A (2009) Labelling and targeted ablation of specific bipolar cell types in the zebrafish retina. BMC Neurosci 10:107.
53. Zhdanova IV (2011) Sleep and its regulation in zebrafish. Rev Neurosci 22:27-36.
54. Zhdanova IV, Wang SY, Leclair OU, Danilova NP (2001) Melatonin promotes sleep-like state in zebrafish. Brain Res 903:263-268.
55. Zimmerman JE, Naidoo N, Raizen DM, Pack AI (2008) Conservation of sleep: insights from non-mammalian model systems. Trends Neurosci 31:371-376.