Evolutionarily conserved regulation of hypocretin neuron specification by Lhx9

Development (Cambridge)

Volumn 142, Issue 6, 2015, Pages 1113-1124

  Liu, Justin ^a   Merkle, Florian T ^b,c   Gandhi, Avni V ^a   Gagnon, James A ^b   Woods, Ian G ^b,f   Chiu, Cindy N ^a   Shimogori, Tomomi ^d   Schier, Alexander F ^b,c,e   Prober, David A ^a  

^a California Institute of Technology   (United States)

^b Harvard University   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

^d RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^e HARVARD MEDICAL SCHOOL   (United States)

^f ITHACA COLLEGE   (United States)

Author keywords

Hypocretin; Lhx9; Zebrafish

Indexed keywords

OREXIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LHX9; UNCLASSIFIED DRUG; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; LHX9 PROTEIN, ZEBRAFISH; NEUROPEPTIDE; PRIMER DNA; SIGNAL PEPTIDE; ZEBRAFISH PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; BRAIN REGION; CLINICAL FEATURE; CONTROLLED STUDY; GENE EXPRESSION; GENE OVEREXPRESSION; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MICROARRAY ANALYSIS; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; ZEBRA FISH; ANIMAL; CELL SEPARATION; EMBRYOLOGY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HIGH THROUGHPUT SCREENING; METABOLISM; MOLECULAR CLONING; NERVE CELL; PHYSIOLOGY; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC ANIMAL;

DANIO RERIO;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL SEPARATION; CLONING, MOLECULAR; DNA PRIMERS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GREEN FLUORESCENT PROTEINS; HIGH-THROUGHPUT SCREENING ASSAYS; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICROARRAY ANALYSIS; NEURONS; NEUROPEPTIDES; OREXINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84930513097     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.117424     Document Type: Article

References (57)

1. Appelbaum, L., Wang, G. X., Maro, G. S., Mori, R., Tovin, A., Marin, W., Yokogawa, T., Kawakami, K., Smith, S. J., Gothilf, Y. et al. (2009). Sleep-wake regulation and hypocretin-melatonin interaction in zebrafish. Proc. Natl. Acad. Sci. USA 106, 21942-21947.
2. Arias-Carrioń, O. and Murillo-Rodrıǵuez, E. (2014). Effects of hypocretin/orexin cell transplantation on narcoleptic-like sleep behavior in rats. PLoS ONE 9, e95342.
3. Birk, O. S., Casiano, D. E., Wassif, C. A., Cogliati, T., Zhao, L., Zhao, Y., Grinberg, A., Huang, S., Kreidberg, J. A., Parker, K. L., et al. (2000). The LIM homeobox gene Lhx9 is essential for mouse gonad formation. Nature 403, 909-913.
4. Blackshaw, S., Scholpp, S., Placzek, M., Ingraham, H., Simerly, R. and Shimogori, T. (2010). Molecular pathways controlling development of thalamus and hypothalamus: from neural specification to circuit formation. J. Neurosci. 30, 14925-14930.
5. Bonnavion, P. and de Lecea, L. (2010). Hypocretins in the control of sleep and wakefulness. Curr. Neurol. Neurosci. Rep. 10, 174-179.
6. Carninci, P., Kasukawa, T., Katayama, S., Gough, J., Frith, M. C., Maeda, N., Oyama, R., Ravasi, T., Lenhard, B., Wells, C. et al. (2005). The transcriptional landscape of the mammalian genome. Science 309, 1559-1563.
7. Chartrel, N., Dujardin, C., Anouar, Y., Leprince, J., Decker, A., Clerens, S., Do-Reǵo, J.-C., Vandesande, F., Llorens-Cortes, C., Costentin, J. et al. (2003). Identification of 26RFa, a hypothalamic neuropeptide of the RFamide peptide family with orexigenic activity. Proc. Natl. Acad. Sci. USA 100, 15247-15252.
8. Chiu, C. N. and Prober, D. A. (2013). Regulation of zebrafish sleep and arousal states: current and prospective approaches. Front. Neural Circuits 7, 58.
9. Chou, T. C., Lee, C. E., Lu, J., Elmquist, J. K., Hara, J., Willie, J. T., Beuckmann, C. T., Chemelli, R. M., Sakurai, T., Yanagisawa, M. et al. (2001). Orexin (hypocretin) neurons contain dynorphin. J. Neurosci. 21, RC168.
10. Cvetkovic-Lopes, V., Bayer, L., Dorsaz, S., Maret, S., Pradervand, S., Dauvilliers, Y., Lecendreux, M., Lammers, G.-J., Donjacour, C. E. H. M., Du Pasquier, R. A. et al. (2010). Elevated Tribbles homolog 2-specific antibody levels in narcolepsy patients. J. Clin. Invest. 120, 713-719.
11. Dalal, J., Roh, J. H., Maloney, S. E., Akuffo, A., Shah, S., Yuan, H., Wamsley, B., Jones, W. B., Strong, C. d. G., Gray, P. A. et al. (2013). Translational profiling of hypocretin neurons identifies candidate molecules for sleep regulation. Genes Dev. 27, 565-578.
12. Dauvilliers, Y., Arnulf, I. and Mignot, E. (2007). Narcolepsy with cataplexy. Lancet 369, 499-511.
13. Elbaz, I., Yelin-Bekerman, L., Nicenboim, J., Vatine, G. and Appelbaum, L. (2012). Genetic ablation of hypocretin neurons alters behavioral state transitions in zebrafish. J. Neurosci. 32, 12961-12972.
14. Elbaz, I., Foulkes, N. S., Gothilf, Y. and Appelbaum, L. (2013). Circadian clocks, rhythmic synaptic plasticity and the sleep-wake cycle in zebrafish. Front. Neural Circuits 7, 9.
15. Faraco, J. H., Appelbaum, L., Marin, W., Gaus, S. E., Mourrain, P. and Mignot, E. (2006). Regulation of hypocretin (orexin) expression in embryonic zebrafish. J. Biol. Chem. 281, 29753-29761.
16. Gagnon, J. A., Valen, E., Thyme, S. B., Huang, P., Ahkmetova, L., Pauli, A., Montague, T. G., Zimmerman, S., Richter, C. and Schier, A. F. (2014). Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs. PLoS ONE 9, e98186.
17. Gibson, D. G., Young, L., Chuang, R.-Y., Venter, J. C., Hutchison, C. A. and Smith, H. O. (2009). Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343-345.
18. Grove, E. A., Tole, S., Limon, J., Yip, L. and Ragsdale, C. W. (1998). The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 125, 2315-2325.
19. Halloran, M. C., Sato-Maeda, M., Warren, J. T., Su, F., Lele, Z., Krone, P. H., Kuwada, J. Y. and Shoji, W. (2000). Laser-induced gene expression in specific cells of transgenic zebrafish. Development 127, 1953-1960.
20. Hanisch, A., Holder, M. V., Choorapoikayil, S., Gajewski, M., Ozbudak, E. M. and Lewis, J. (2012). The elongation rate of RNA polymerase II in zebrafish and its significance in the somite segmentation clock. Development 140, 444-453.
21. Higashijima, S., Hotta, Y. and Okamoto, H. (2000). Visualization of cranial motor neurons in live transgenic zebrafish expressing green fluorescent protein under the control of the islet-1 promoter/enhancer. J. Neurosci. 20, 206-218.
22. Hobert, O. and Westphal, H. (2000). Functions of LIM-homeobox genes. Trends Genet. 16, 75-83.
23. Honda, M., Eriksson, K. S., Zhang, S., Tanaka, S., Lin, L., Salehi, A., Hesla, P. E., Maehlen, J., Gaus, S. E., Yanagisawa, M. et al. (2009). IGFBP3 colocalizes with and regulates hypocretin (orexin). PLoS ONE 4, e4254.
24. Horvath, T. L., Peyron, C., Diano, S., Ivanov, A., Aston-Jones, G., Kilduff, T. S. and van den Pol, A. N. (1999). Hypocretin (orexin) activation and synaptic innervation of the locus coeruleus noradrenergic system. J. Comp. Neurol. 415, 145-159.
25. Hwang, W. Y., Fu, Y., Reyon, D., Maeder, M. L., Tsai, S. Q., Sander, J. D., Peterson, R. T., Yeh, J.-R. J. and Joung, J. K. (2013). Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat. Biotechnol. 31, 227-229.
26. Jao, L.-E., Wente, S. R. and Chen, W. (2013). Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc. Natl. Acad. Sci. USA 110, 13904-13909.
27. Kaslin, J., Nystedt, J. M., Ö stergård, 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.
28. Kosman, D., Mizutani, C. M., Lemons, D., Cox, W. G., McGinnis, W. and Bier, E. (2004). Multiplex detection of RNA expression in Drosophila embryos. Science 305, 846.
29. Koyama, M., Kinkhabwala, A., Satou, C., Higashijima, S.-i. and Fetcho, J. (2011). Mapping a sensory-motor network onto a structural and functional ground plan in the hindbrain. Proc. Natl. Acad. Sci. USA 108, 1170-1175.
30. Kucenas, S., Soto, F., Cox, J. A. and Voigt, M. M. (2006). Selective labeling of central and peripheral sensory neurons in the developing zebrafish using P2X3 receptor subunit transgenes. Neuroscience 138, 641-652.
31. Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J. et al. (2006). Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168-176.
32. Machluf, Y., Gutnick, A. and Levkowitz, G. (2011). Development of the zebrafish hypothalamus. Ann. N. Y. Acad. Sci. 1220, 93-105.
33. Manoli, M. and Driever, W. (2012). Fluorescence-activated cell sorting (FACS) of fluorescently tagged cells from zebrafish larvae for RNA isolation. Cold Spring Harb. Protoc. 2012, ppii: pdb.prot069633.
34. Matsui, A., Yoshida, A. C., Kubota, M., Ogawa, M. and Shimogori, T. (2011). Mouse in utero electroporation: controlled spatiotemporal gene transfection. J. Vis. Exp. e3024.
35. Montague, T. G., Cruz, J. M., Gagnon, J. A., Church, G. M. and Valen, E. (2014). CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res. 42, W401-W407.
36. Onishi, A., Peng, G.-H., Poth, E. M., Lee, D. A., Chen, J., Alexis, U., de Melo, J., Chen, S. and Blackshaw, S. (2010). The orphan nuclear hormone receptor ERRβ controls rod photoreceptor survival. Proc. Natl. Acad. Sci. USA 107, 11579-11584.
37. Peukert, D., Weber, S., Lumsden, A. and Scholpp, S. (2011). Lhx2 and Lhx9 determine neuronal differentiation and compartition in the caudal forebrain by regulating Wnt signaling. PLoS Biol. 9, e1001218.
38. Peyron, C., Faraco, J., Rogers, W., Ripley, B., Overeem, S., Charnay, Y., Nevsimalova, S., Aldrich, M., Reynolds, D., Albin, R. et al. (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.
39. 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.
40. Prober, D. A., Zimmerman, S., Myers, B. R., McDermott, B. M., Kim, S.-H., Caron, S., Rihel, J., Solnica-Krezel, L., Julius, D., Hudspeth, A. J. et al. (2008). Zebrafish TRPA1 channels are required for chemosensation but not for thermosensation or mechanosensory hair cell function. J. Neurosci. 28, 10102-10110.
41. 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.
42. Rosin, D. L., Weston, M. C., Sevigny, C. P., Stornetta, R. L. and Guyenet, P. G. (2003). Hypothalamic orexin (hypocretin) neurons express vesicular glutamate transporters VGLUT1 or VGLUT2. J. Comp. Neurol. 465, 593-603.
43. Sagasti, A., Guido, M. R., Raible, D. W. and Schier, A. F. (2005). Repulsive interactions shape the morphologies and functional arrangement of zebrafish peripheral sensory arbors. Curr. Biol. 15, 804-814.
44. Sato, T., Takahoko, M. and Okamoto, H. (2006). HuC:Kaede, a useful tool to label neural morphologies in networks in vivo. Genesis 44, 136-142.
45. Sawai, N., Ueta, Y., Nakazato, M. and Ozawa, H. (2010). Developmental and aging change of orexin-A and -B immunoreactive neurons in the male rat hypothalamus. Neurosci. Lett. 468, 51-55.
46. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682.
47. Schmittgen, T. D. and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101-1108.
48. Shimogori, T., Lee, D. A., Miranda-Angulo, A., Yang, Y., Wang, H., Jiang, L., Yoshida, A. C., Kataoka, A., Mashiko, H., Avetisyan, M. et al. (2010). A genomic atlas of mouse hypothalamic development. Nat. Neurosci. 13, 767-775.
49. Takayasu, S., Sakurai, T., Iwasaki, S., Teranishi, H., Yamanaka, A., Williams, S. C., Iguchi, H., Kawasawa, Y. I., Ikeda, Y., Sakakibara, I. et al. (2006). A neuropeptide ligand of the G protein-coupled receptor GPR103 regulates feeding, behavioral arousal, and blood pressure in mice. Proc. Natl. Acad. Sci. USA 103, 7438-7443.
50. Tessmar-Raible, K., Raible, F., Christodoulou, F., Guy, K., Rembold, M., Hausen, H. and Arendt, D. (2007). Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Cell 129, 1389-1400.
51. Thannickal, T. C., Moore, R. Y., Nienhuis, R., Ramanathan, L., Gulyani, S., Aldrich, M., Cornford, M. and Siegel, J. M. (2000). Reduced number of hypocretin neurons in human narcolepsy. Neuron 27, 469-474.
52. Thisse, C. and Thisse, B. (2008). High-resolution in situ hybridization to wholemount zebrafish embryos. Nat. Protoc. 3, 59-69.
53. Tsujino, N. and Sakurai, T. (2009). Orexin/hypocretin: a neuropeptide at the interface of sleep, energy homeostasis, and reward system. Pharmacol. Rev. 61, 162-176.
54. Westerfield, M. (1993). The Zebrafish Book. A Guide for The Laboratory Use of Zebrafish (Danio rerio), 4th edn. Eugene, OR: University of Oregon Press.
55. Wilhelm, D. and Englert, C. (2002). The Wilms tumor suppressor WT1 regulates early gonad development by activation of Sf1. Genes Dev. 16, 1839-1851.
56. Wilson, S. W. and Houart, C. (2004). Early steps in the development of the forebrain. Dev. Cell 6, 167-181.
57. Yamamoto, T., Miyazaki, R. and Yamada, T. (2009). Intracerebroventricular administration of 26RFa produces an analgesic effect in the rat formalin test. Peptides 30, 1683-1688.