The histaminergic system regulates wakefulness and orexin/hypocretin neuron development via histamine receptor H1 in zebrafish

FASEB Journal

Volumn 25, Issue 12, 2011, Pages 4338-4347

  Sundvik, Maria ^a   Kudo, Hisaaki ^a   Toivonen, Pauliina ^a,b   Rozov, Stanislav ^a   Chen, Yu Chia ^a   Panula, Pertti ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Dorsal telencephalon; Locomotor activity; Sleep disorders; Tracing

Indexed keywords

HISTAMINE RECEPTOR; HISTAMINE RECEPTOR H1; HISTAMINE RECEPTOR H3; HISTIDINE DECARBOXYLASE; MESSENGER RNA; OREXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL COUNT; CONTROLLED STUDY; ENZYME INHIBITION; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TELENCEPHALON; WAKEFULNESS; ZEBRA FISH;

AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; BASE SEQUENCE; DNA PRIMERS; GENE EXPRESSION; HISTAMINE; HISTIDINE DECARBOXYLASE; HYPOTHALAMUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LARVA; LIGHT; NEURONS; NEUROPEPTIDES; RECEPTORS, HISTAMINE H1; RECEPTORS, HISTAMINE H3; TELENCEPHALON; WAKEFULNESS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 82655181503     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-188268     Document Type: Article

References (58)

1. Cirelli, C. (2009) The genetic and molecular regulation of sleep: from fruit flies to humans. Nat. Rev. Neurosci. 10, 549-560
2. Anaclet, C., Parmentier, R., Ouk, K., Guidon, G., Buda, C., Sastre, J. P., Akaoka, H., Sergeeva, O. A., Yanagisawa, M., Ohtsu, H., Franco, P., Haas, H. L., and Lin, J. S. (2009) Orexin/ hypocretin and histamine: distinct roles in the control of wakefulness demonstrated using knock-out mouse models. J. Neurosci. 29, 14423-14438
3. Panula, P., Yang, H. Y., and Costa, E. (1984) Histamine-containing neurons in the rat hypothalamus. Proc. Natl. Acad. Sci. U. S. A. 81, 2572-2576
4. Watanabe, T., Taguchi, Y., Shiosaka, S., Tanaka, J., Kubota, H., Terano, Y., Tohyama, M., and Wada, H. (1984) Distribution of the histaminergic neuron system in the central nervous system of rats; a fluorescent immunohistochemical analysis with histidine decarboxylase as a marker. Brain Res. 295, 13-25 (Pubitemid 14155851)
5. Haas, H., and Panula, P. (2003) The role of histamine and the tuberomamillary nucleus in the nervous system. Nat. Rev. Neurosci. 4, 121-130 (Pubitemid 37271382)
6. Lin, J. S., Hou, Y., Sakai, K., and Jouvet, M. (1996) Histaminergic descending inputs to the mesopontine tegmentum and their role in the control of cortical activation and wakefulness in the cat. J. Neurosci. 16, 1523-1537 (Pubitemid 26145931)
7. Passani, M. B., Lin, J. S., Hancock, A., Crochet, S., and Blandina, P. (2004) The histamine H3 receptor as a novel therapeutic target for cognitive and sleep disorders. Trends Pharmacol. Sci. 25, 618-625 (Pubitemid 39458167)
8. Monti, J. M., Pellejero, T., and Jantos, H. (1986) Effects of H1-and H2-histamine receptor agonists and antagonists on sleep and wakefulness in the rat. J. Neural Trans. 66, 1-11 (Pubitemid 16011942)
9. Monti, J. M., Jantos, H., Boussard, M., Altier, H., Orellana, C., and Olivera, S. (1991) Effects of selective activation or blockade of the histamine H3 receptor on sleep and wakefulness. Eur. J. Pharmacol. 205, 283-287
10. Sakurai, T., Amemiya, A., Ishii, M., Matsuzaki, I., Chemelli, R. M., Tanaka, H., Williams, S. C., Richardson, J. A., Kozlowski, G. P., Wilson, S., Arch, J. R., Buckingham, R. E., Haynes, A. C., Carr, S. A., Annan, R. S., McNulty, D. E., Liu, W. S., Terrett, J. A., Elshourbagy, N. A., Bergsma, D. J., and Yanagisawa, M. (1998) Orexins and orexin receptors: A family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 573-585 (Pubitemid 28101119)
11. De Lecea, L., Kilduff, T. S., Peyron, C., Gao, X., Foye, P. E., Danielson, P. E., Fukuhara, C., Battenberg, E. L., Gautvik, V. T., Bartlett, F. S., 2nd, Frankel, W. N., van den Pol, A. N., Bloom, F. E., Gautvik, K. M., and Sutcliffe, J. G. (1998) The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc. Natl. Acad. Sci. U. S. A. 95, 322-327 (Pubitemid 28103952)
12. Peyron, C., Tighe, D. K., van den Pol, A. N., de Lecea, L., Heller, H. C., Sutcliffe, J. G., and Kilduff, T. S. (1998) Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci. 18, 9996-10015 (Pubitemid 28543775)
13. Kaslin, J., Nystedt, J. M., Ostergard, M., Peitsaro, N., and Panula, P. (2004) The orexin/hypocretin system in zebrafish is connected to the aminergic and cholinergic systems. J. Neurosci. 24, 2678-2689 (Pubitemid 38380944)
14. 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, G. J., Bouras, C., Kucherlapati, R., Nishino, S., and 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
15. Nishino, S., Sakurai, E., Nevsimalova, S., Yoshida, Y., Watanabe, T., Yanai, K., and Mignot, E. (2009) Decreased CSF histamine in narcolepsy with and without low CSF hypocretin-1 in comparison to healthy controls. Sleep 32, 175-180
16. O'Malley, D. M., Kao, Y. H., and Fetcho, J. R. (1996) Imaging the functional organization of zebrafish hindbrain segments during escape behaviors Neuron 17, 1145-1155 (Pubitemid 27021100)
17. Gahtan, E., Tanger, P., and Baier, H. (2005) Visual prey capture in larval zebrafish is controlled by identified reticulospinal neurons downstream of the tectum. J. Neurosci. 25, 9294-9303 (Pubitemid 41500838)
18. Burgess, H. A., and Granato, M. (2007) Modulation of locomotor activity in larval zebrafish during light adaptation. J. Exp. Biol. 210, 2526-2539 (Pubitemid 47235044)
19. Burgess, H. A., and Granato, M. (2007) Sensorimotor gating in larval zebrafish. J. Neurosci. 27, 4984-4994 (Pubitemid 46699065)
20. Burgess, H. A., Johnson, S. L., and Granato, M. (2009) Unidirectional startle responses and disrupted left-right co-ordination of motor behaviors in robo3 mutant zebrafish. Genes Brain Behav. 8, 500-511
21. Burgess, H. A., Schoch, H., and Granato, M. (2010) Distinct retinal pathways drive spatial orientation behaviors in zebrafish navigation. Curr. Biol. 20, 381-386
22. Peitsaro, N., Sundvik, M., Anichtchik, O. V., Kaslin, J., and Panula, P. (2007) Identification of zebrafish histamine H1, H2 and H3 receptors and effects of histaminergic ligands on behavior. Biochem. Pharmacol. 73, 1205-1214 (Pubitemid 46413182)
23. Kaslin, J., and Panula, P. (2001) Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio). J. Comp. Neurol. 440, 342-377 (Pubitemid 33041750)
24. Sallinen, V., Torkko, V., Sundvik, M., Reenila, I., Khrustalyov, D., Kaslin, J., and Panula, P. (2009) MPTP and MPP+ target specific aminergic cell populations in larval zebrafish. J. Neurochem. 108, 719-731
25. Sallinen, V., Sundvik, M., Reenila, I., Peitsaro, N., Khrustalyov, D., Anichtchik, O., Toleikyte, G., Kaslin, J., and Panula, P. (2009) Hyperserotonergic phenotype after monoamine oxidase inhibition in larval zebrafish. J. Neurochem. 109, 403-415
26. Kobbert, C., Apps, R., Bechmann, I., Lanciego, J. L., Mey, J., and Thanos, S. (2000) Current concepts in neuroanatomical tracing. Prog. Neurobiol. 62, 327-351 (Pubitemid 30336472)
27. Eriksson, K. S., Peitsaro, N., Karlstedt, K., Kaslin, J., and Panula, P. (1998) Development of the histaminergic neurons and expression of histidine decarboxylase mRNA in the zebrafish brain in the absence of all peripheral histaminergic systems. Eur. J. Neurosci. 10, 3799-3812 (Pubitemid 29073936)
28. Keegan, B. R., Feldman, J. L., Lee, D. H., Koos, D. S., Ho, R. K., Stainier, D. Y., and Yelon, D. (2002) The elongation factors Pandora/Spt6 and Foggy/Spt5 promote transcription in the zebrafish embryo. Development 129, 1623-1632 (Pubitemid 34874180)
29. Thisse, C., and Thisse, B. (2008) High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protocols 3, 59-69
30. Chen, Y. C., Priyadarshini, M., and Panula, P. (2009) Complementary developmental expression of the two tyrosine hydroxylase transcripts in zebrafish. Histochem. Cell Biol. 132, 375-381
31. Kudo, H., Liu, J., Jansen, E. J., Ozawa, A., Panula, P., Martens, G. J., and Lindberg, I. (2009) Identification of proSAAS homologs in lower vertebrates: conservation of hydrophobic helices and convertase-inhibiting sequences. Endocrinology 150, 1393-1399
32. Yokogawa, T., Marin, W., Faraco, J., Pezeron, G., Appelbaum, L., Zhang, J., Rosa, F., Mourrain, P., and Mignot, E. (2007) Characterization of sleep in zebrafish and insomnia in hypocretin receptor mutants. PLoS Biol. 5, e277
33. Higashijima, S., Mandel, G., and Fetcho, J. R. (2004) Distribution of prospective glutamatergic, glycinergic, and GABAergic neurons in embryonic and larval zebrafish. J. Comp. Neurol. 480, 1-18
34. Auvinen, S., and Panula, P. (1988) Development of histamine- immunoreactive neurons in the rat brain. J. Comp. Neurol. 276, 289-303
35. Panula, P., Airaksinen, M. S., Pirvola, U., and Kotilainen, E. (1990) A histamine-containing neuronal system in human brain. Neuroscience 34, 127-132 (Pubitemid 20097900)
36. Panula, P., Pirvola, U., Auvinen, S., and Airaksinen, M. S. (1989) Histamine-immunoreactive nerve fibers in the rat brain. Neuroscience 28, 585-610 (Pubitemid 19081018)
37. Robu, M. E., Larson, J. D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S. A., and Ekker, S. C. (2007) P53 activation by knockdown technologies. PLoS Genet. 3, e78
38. Eisen, J. S., and Smith, J. C. (2008) Controlling morpholino experiments: don't stop making antisense. Development 135, 1735-1743
39. Vargas, J. P., Lopez, J. C., and Portavella, M. (2009) What are the functions of fish brain pallium? Brain Res. Bull. 79, 436-440
40. Eriksson, K. S., Sergeeva, O., Brown, R. E., and Haas, H. L. (2001) Orexin/hypocretin excites the histaminergic neurons of the tuberomammillary nucleus. J. Neurosci. 21, 9273-9279 (Pubitemid 33096871)
41. Peitsaro, N., Kaslin, J., Anichtchik, O. V., and Panula, P. (2003) Modulation of the histaminergic system and behaviour by alpha- fluoromethylhistidine in zebrafish. J. Neurochem. 86, 432-441 (Pubitemid 36842442)
42. Moree, W. J., Li, B. F., Jovic, F., Coon, T., Yu, J., Gross, R. S., Tucci, F., Marinkovic, D., Zamani-Kord, S., Malany, S., Bradbury, M. J., Hernandez, L. M., O'Brien, Z., Wen, J., Wang, H., Hoare, S. R., Petroski, R. E., Sacaan, A., Madan, A., Crowe, P. D., and Beaton, G. (2009) Characterization of novel selective H1-antihistamines for clinical evaluation in the treatment of insomnia. J. Med. Chem. 52, 5307-5310
43. Pillot, C., Heron, A., Cochois, V., Tardivel-Lacombe, J., Ligneau, X., Schwartz, J. C., and Arrang, J. M. (2002) A detailed mapping of the histamine H(3) receptor and its gene transcripts in rat brain. Neuroscience 114, 173-193 (Pubitemid 35247499)
44. Haas, H. L., Sergeeva, O. A., and Selbach, O. (2008) Histamine in the nervous system. Physiol. Rev. 88, 1183-1241
45. Jin, C. Y., and Panula, P. (2005) The laminar histamine receptor system in human prefrontal cortex suggests multiple levels of histaminergic regulation. Neuroscience 132, 137-149 (Pubitemid 40380721)
46. Jin, C. Y., Anichtchik, O., and Panula, P. (2009) Altered histamine H3 receptor radioligand binding in post-mortem brain samples from subjects with psychiatric diseases. Brit. J. Pharmacol. 157, 118-129
47. Emran, F., Rihel, J., and Dowling, J. E. (2008) A behavioral assay to measure responsiveness of zebrafish to changes in light intensities. JoVE 20, 923 doi: 10.3791/923
48. Perala, N., Peitsaro, N., Sundvik, M., Koivula, H., Sainio, K., Sariola, H., Panula, P., and Immonen, T. (2010) Conservation, expression, and knockdown of zebrafish plxnb2a and plxnb2b. Dev. Dyn. 239, 2722-2734
49. Mueller, T., Wullimann, M. F., and Guo, S. (2008) Early teleostean basal ganglia development visualized by zebrafish Dlx2a, Lhx6, Lhx7, Tbr2 (eomesa), and GAD67 gene expression. J. Comp. Neurol. 507, 1245-1257 (Pubitemid 351288024)
50. Prober, D. A., Rihel, J., Onah, A. A., Sung, R. J., and Schier, A. F. (2006) Hypocretin/orexin overexpression induces an insomnia-like phenotype in zebrafish. J. Neurosci. 26, 13400-13410 (Pubitemid 46011651)
51. Naumann, E. A., Kampff, A. R., Prober, D. A., Schier, A. F., and Engert, F. (2010) Monitoring neural activity with bioluminescence during natural behavior. Nat. Neurosci. 13, 513-520
52. Huang, Z. L., Qu, W. M., Li, W. D., Mochizuki, T., Eguchi, N., Watanabe, T., Urade, Y., and Hayaishi, O. (2001) Arousal effect of orexin A depends on activation of the histaminergic system. Proc. Natl. Acad. Sci. U. S. A. 98, 9965-9970 (Pubitemid 32769411)
53. Bayer, L., Eggermann, E., Serafin, M., Saint-Mleux, B., Machard, D., Jones, B., and Muhlethaler, M. (2001) Orexins (hypocretins) directly excite tuberomammillary neurons. Eur. J. Neurosci. 14, 1571-1575 (Pubitemid 35463724)
54. Yamanaka, A., Tsujino, N., Funahashi, H., Honda, K., Guan, J. L., Wang, Q. P., Tominaga, M., Goto, K., Shioda, S., and Sakurai, T. (2002) Orexins activate histaminergic neurons via the orexin 2 receptor. Biochem. Biophys. Res. Commun. 290, 1237-1245 (Pubitemid 34694437)
55. Kanbayashi, T., Kodama, T., Kondo, H., Satoh, S., Inoue, Y., Chiba, S., Shimizu, T., and Nishino, S. (2009) CSF histamine contents in narcolepsy, idiopathic hypersomnia and obstructive sleep apnea syndrome. Sleep 32, 181-187
56. Scammell, T. E., and Mochizuki, T. (2009) Is low histamine a fundamental cause of sleepiness in narcolepsy and idiopathic hypersomnia? Sleep 32, 133-134
57. Guo, R. X., Anaclet, C., Roberts, J. C., Parmentier, R., Zhang, M., Guidon, G., Buda, C., Sastre, J. P., Feng, J. Q., Franco, P., Brown, S. H., Upton, N., Medhurst, A. D., and Lin, J. S. (2009) Differential effects of acute and repeat dosing with the H3 antagonist GSK189254 on the sleep-wake cycle and narcoleptic episodes in ox-/- mice. Br. J. Pharmacol. 157, 104 -117
58. Lin, L., Wisor, J., Shiba, T., Taheri, S., Yanai, K., Wurts, S., Lin, X., Vitaterna, M., Takahashi, J., Lovenberg, T. W., Koehl, M., Uhl, G., Nishino, S., and Mignot, E. (2002) Measurement of hypocretin/orexin content in the mouse brain using an enzyme immunoassay: the effect of circadian time, age and genetic background. Peptides 23, 2203-2211 (Pubitemid 36092055)