The circadian clock regulates autophagy directly through the nuclear hormone receptor Nr1d1/Rev-erbα and indirectly via Cebpb/(C/ebpβ) in zebrafish

Autophagy

Volumn 12, Issue 8, 2016, Pages 1292-1309

  Huang, Guodong ^a   Zhang, Fanmiao ^a   Ye, Qiang ^a   Wang, Han ^a  

^a SOOCHOW UNIVERSITY   (China)

Author keywords

autophagy; Cebpb (C ebp ); circadian; Nr1d1 Rev erb ; Per1b; zebrafish

Indexed keywords

BECLIN 1; CEBPB PROTEIN; NUCLEAR RECEPTOR NR1D1; PROTEIN; PROTEIN BNIP3; UNCLASSIFIED DRUG; CCAAT ENHANCER BINDING PROTEIN BETA; CIRCADIAN RHYTHM SIGNALING PROTEIN; NR1D1 PROTEIN, ZEBRAFISH; PER1B PROTEIN, ZEBRAFISH; TRANSCRIPTOME; ZEBRAFISH PROTEIN;

ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CIRCADIAN RHYTHM; CONTROLLED STUDY; DNA SEQUENCE; FEMALE; LOCOMOTION; MALE; MUTAGENESIS; NONHUMAN; NUTRITIONAL STATUS; OBESITY; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROCESSING; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; ZEBRA FISH; ANIMAL; CELL NUCLEUS; EMBRYOLOGY; GENE EXPRESSION REGULATION; LIVER; METABOLISM; MUTATION; SITE DIRECTED MUTAGENESIS; UPREGULATION;

ANIMALS; AUTOPHAGY; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL NUCLEUS; CIRCADIAN CLOCKS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LIVER; MALE; MUTAGENESIS; MUTAGENESIS, SITE-DIRECTED; MUTATION; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP D, MEMBER 1; PERIOD CIRCADIAN PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTOME; UP-REGULATION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84976312619     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2016.1183843     Document Type: Article

References (77)

1. T.C.Walther, R.V.Farese, Jr. Lipid droplets and cellular lipid metabolism. Ann Rev Biochem 2012; 81:687-714; PMID:22524315; http://dx.doi.org/10.1146/annurev-biochem-061009-102430
2. M.E.Hughes, J.B.Hogenesch, K.Kornacker. JTK_CYCLE:an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J Biol Rhythms 2010; 25:372-80; PMID:20876817; http://dx.doi.org/10.1177/0748730410379711
3. S.Panda, J.B.Hogenesch, S.A.Kay. Circadian rhythms from flies to human. Nature 2002; 417:329-35; PMID:12015613; http://dx.doi.org/10.1038/417329a
4. H.R.Ueda, W.Chen, A.Adachi, H.Wakamatsu, S.Hayashi, T.Takasugi, M.Nagano, K.Nakahama, Y.Suzuki, S.Sugano, et al. A transcription factor response element for gene expression during circadian night. Nature 2002; 418:534-9; PMID:12152080; http://dx.doi.org/10.1038/nature00906
5. C.H.Ko, J.S.Takahashi. Molecular components of the mammalian circadian clock. Hum Mol Genetics 2006; 15 Spec No 2:R271-7; http://dx.doi.org/10.1093/hmg/ddl207
6. H.Cho, X.Zhao, M.Hatori, R.T.Yu, G.D.Barish, M.T.Lam, L.W.Chong, L.DiTacchio, A.R.Atkins, C.K.Glass, et al. Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature 2012; 485:123-7; PMID:22460952; http://dx.doi.org/10.1038/nature11048
7. Y.Kumaki, M.Ukai-Tadenuma, K.D.Uno, J.Nishio, K.H.Masumoto, M.Nagano, T.Komori, Y.Shigeyoshi, J.B.Hogenesch, H.R.Ueda, et al. Analysis and synthesis of high-amplitude Cis-elements in the mammalian circadian clock. Proc Natl Acad Sci U S A 2008; 105:14946-51; PMID:18815372; http://dx.doi.org/10.1073/pnas.0802636105
8. N.Mizushima, B.Levine, A.M.Cuervo, D.J.Klionsky. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069-75; PMID:18305538; http://dx.doi.org/10.1038/nature06639
9. J.D.Rabinowitz, E.White. Autophagy and metabolism. Science 2010; 330:1344-8; PMID:21127245; http://dx.doi.org/10.1126/science.1193497
10. P.M.Wong, C.Puente, I.G.Ganley, X.Jiang. The ULK1 complex:sensing nutrient signals for autophagy activation. Autophagy 2013; 9:124-37; PMID:23295650; http://dx.doi.org/10.4161/auto.23323
11. I.G.Ganley, H.Lam du, J.Wang, X.Ding, S.Chen, X.Jiang. ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 2009; 284:12297-305; PMID:19258318; http://dx.doi.org/10.1074/jbc.M900573200
12. A.Kuma, N.Mizushima. Physiological role of autophagy as an intracellular recycling system:with an emphasis on nutrient metabolism. Seminars Cell Dev Biol 2010; 21:683-90; http://dx.doi.org/10.1016/j.semcdb.2010.03.002
13. X.H.Liang, S.Jackson, M.Seaman, K.Brown, B.Kempkes, H.Hibshoosh, B.Levine. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999; 402:672-6; PMID:10604474; http://dx.doi.org/10.1038/45257
14. U.Pfeifer, H.Scheller. A morphometric study of cellular autophagy including diurnal variations in kidney tubules of normal rats. J Cell Biol 1975; 64:608-21; PMID:1171105; http://dx.doi.org/10.1083/jcb.64.3.608
15. C.E.Reme, M.Sulser. Diurnal variation of autophagy in rod visual cells in the rat. Albrecht Von Graefes Archiv Klin Exp Ophthalmol 1977; 203:261-70; PMID:303474; http://dx.doi.org/10.1007/BF00409832
16. D.Ma, S.Panda, J.D.Lin. Temporal orchestration of circadian autophagy rhythm by C/EBPbeta. EMBO J 2011; 30:4642-51; PMID:21897364; http://dx.doi.org/10.1038/emboj.2011.322
17. H.Duez, J.N.van der Veen, C.Duhem, B.Pourcet, T.Touvier, C.Fontaine, B.Derudas, E.Baugé, R.Havinga, V.W.Bloks, et al. Regulation of bile acid synthesis by the nuclear receptor Rev-erbalpha. Gastroenterol 2008; 135:689-98; http://dx.doi.org/10.1053/j.gastro.2008.05.035
18. C.Fontaine, G.Dubois, Y.Duguay, T.Helledie, N.Vu-Dac, P.Gervois, F.Soncin, S.Mandrup, J.C.Fruchart, J.Fruchart-Najib, et al. The orphan nuclear receptor Rev-Erbalpha is a peroxisome proliferator-activated receptor (PPAR) gamma target gene and promotes PPARgamma-induced adipocyte differentiation. J Biol Chem 2003; 278:37672-80; PMID:12821652; http://dx.doi.org/10.1074/jbc.M304664200
19. C.Fontaine, E.Rigamonti, B.Pourcet, H.Duez, C.Duhem, J.C.Fruchart, G.Chinetti-Gbaguidi, B.Staels. The nuclear receptor Rev-erbalpha is a liver X receptor (LXR) target gene driving a negative feedback loop on select LXR-induced pathways in human macrophages. Mol Endocrinol 2008; 22:1797-811; PMID:18511497; http://dx.doi.org/10.1210/me.2007-0439
20. L.Yin, N.Wu, J.C.Curtin, M.Qatanani, N.R.Szwergold, R.A.Reid, G.M.Waitt, D.J.Parks, K.H.Pearce, G.B.Wisely, et al. Rev-erbalpha, a heme sensor that coordinates metabolic and circadian pathways. Sci 2007; 318:1786-9; http://dx.doi.org/10.1126/science.1150179
21. S.Raghuram, K.R.Stayrook, P.Huang, P.M.Rogers, A.K.Nosie, D.B.McClure, L.L.Burris, S.Khorasanizadeh, T.P.Burris, F.Rastinejad. Identification of heme as the ligand for the orphan nuclear receptors REV-ERBalpha and REV-ERBbeta. Nat Structural Mol Biol 2007; 14:1207-13; http://dx.doi.org/10.1038/nsmb1344
22. E.Woldt, Y.Sebti, L.A.Solt, C.Duhem, S.Lancel, J.Eeckhoute, M.K.Hesselink, C.Paquet, S.Delhaye, Y.Shin, et al. Rev-erb-α modulates skeletal muscle oxidative capacity by regulating mitochondrial biogenesis and autophagy. Nat Med 2013; 19:1039-46; PMID:23852339; http://dx.doi.org/10.1038/nm.3213
23. C.He, D.J.Klionsky. Analyzing autophagy in zebrafish. Autophagy 2010; 6:642-4; PMID:20495344; http://dx.doi.org/10.4161/auto.6.5.12092
24. C.He, C.R.Bartholomew, W.Zhou, D.J.Klionsky. Assaying autophagic activity in transgenic GFP-Lc3 and GFP-Gabarap zebrafish embryos. Autophagy 2009; 5:520-6; PMID:19221467; http://dx.doi.org/10.4161/auto.5.4.7768
25. L.Appelbaum, G.X.Wang, G.S.Maro, R.Mori, A.Tovin, W.Marin, T.Yokogawa, K.Kawakami, S.J.Smith, Y.Gothilf, et al. Sleep-wake regulation and hypocretin-melatonin interaction in zebrafish. Proc Natl Acad Sci U S A 2009; 106:21942-7; PMID:19966231; http://dx.doi.org/10.1073/pnas.906637106
26. P.Huang, A.Xiao, M.Zhou, Z.Zhu, S.Lin, B.Zhang. Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol 2011; 29:699-700; PMID:21822242; http://dx.doi.org/10.1038/nbt.1939
27. D.Wang, L.E.Jao, N.Zheng, K.Dolan, J.Ivey, S.Zonies, X.Wu, K.Wu, H.Yang, Q.Meng, et al. Efficient genome-wide mutagenesis of zebrafish genes by retroviral insertions. Proc Natl Acad Sci U S A 2007; 104:12428-33; PMID:17640903; http://dx.doi.org/10.1073/pnas.0705502104
28. E.Wienholds, F.van Eeden, M.Kosters, J.Mudde, R.H.Plasterk, E.Cuppen. Efficient target-selected mutagenesis in zebrafish. Genome Res 2003; 13:2700-7; PMID:14613981; http://dx.doi.org/10.1101/gr.1725103
29. W.Y.Hwang, Y.Fu, D.Reyon, M.L.Maeder, S.Q.Tsai, J.D.Sander, R.T.Peterson, J.R.Yeh, J.K.Joung. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 2013; 31:227-9; PMID:23360964; http://dx.doi.org/10.1038/nbt.2501
30. J.Huang, Z.Zhong, M.Wang, X.Chen, Y.Tan, S.Zhang, W.He, X.He, G.Huang, H.Lu, et al. Circadian modulation of dopamine levels and dopaminergic neuron development contributes to attention deficiency and hyperactive behavior. J Neurosci 2015; 35:2572-87; PMID:25673850; http://dx.doi.org/10.1523/JNEUROSCI.2551-14.2015
31. Y.Tan, J.DeBruyne, G.M.Cahill, D.E.Wells. Identification of a mutation in the Clock1 gene affecting zebrafish circadian rhythms. J Neurogenetics 2008; 22:149-66; http://dx.doi.org/10.1080/01677060802049738
32. M.Wang, Z.Zhong, Y.Zhong, W.Zhang, H.Wang. The Zebrafish period2 protein positively regulates the circadian clock through mediation of retinoic acid receptor (RAR)-related orphan receptor α (Roralpha). J Biol Chem 2015; 290:4367-82; PMID:25544291; http://dx.doi.org/10.1074/jbc.M114.605022
33. K.Kyostila, P.Syrja, V.Jagannathan, G.Chandrasekar, T.S.Jokinen, E.H.Seppala, D.Becker, M.Drögemüller, E.Dietschi, C.Drögemüller, et al. A missense change in the ATG4D gene links aberrant autophagy to a neurodegenerative vacuolar storage disease. PLoS Genetics 2015; 11:e1005169; PMID:25875846; http://dx.doi.org/10.1371/journal.pgen.1005169
34. E.L.Eskelinen. To be or not to be? Examples of incorrect identification of autophagic compartments in conventional transmission electron microscopy of mammalian cells. Autophagy 2008; 4:257-60; PMID:17986849; http://dx.doi.org/; http://dx.doi.org/10.4161/auto.5179
35. F.Delaunay, C.Thisse, O.Marchand, V.Laudet, B.Thisse. An inherited functional circadian clock in zebrafish embryos. Science 2000; 289:297-300; PMID:10894777; http://dx.doi.org/10.1126/science.289.5477.297
36. G.Cretenet, M.Le Clech, F.Gachon. Circadian clock-coordinated 12 Hr period rhythmic activation of the IRE1alpha pathway controls lipid metabolism in mouse liver. Cell Metab 2010; 11:47-57; PMID:20074527; http://dx.doi.org/10.1016/j.cmet.2009.11.002
37. C.He, D.J.Klionsky. Regulation mechanisms and signaling pathways of autophagy. Ann Rev Genetics 2009; 43:67-93; http://dx.doi.org/10.1146/annurev-genet-102808-114910
38. J.Moscat, M.T.Diaz-Meco. p62 at the crossroads of autophagy, apoptosis, and cancer. Cell 2009; 137:1001-4; PMID:19524504; http://dx.doi.org/10.1016/j.cell.2009.05.023
39. S.Lattante, H.de Calbiac, I.Le Ber, A.Brice, S.Ciura, E.Kabashi. Sqstm1 knock-down causes a locomotor phenotype ameliorated by rapamycin in a zebrafish model of ALS/FTLD. Hum Mol Genetics 2015; 24:1682-90; http://dx.doi.org/10.1093/hmg/ddu580
40. E.L.Doyle, N.J.Booher, D.S.Standage, D.F.Voytas, V.P.Brendel, J.K.Vandyk, A.J.Bogdanove. TAL Effector-Nucleotide Targeter (TALE-NT) 2.0:tools for TAL effector design and target prediction. Nucleic Acids Res 2012; 40:W117-22; PMID:22693217; http://dx.doi.org/10.1093/nar/gks608
41. P.Huang, A.Xiao, X.Tong, Y.Zu, Z.Wang, B.Zhang. TALEN construction via “Unit Assembly” method and targeted genome modifications in zebrafish. Methods 2014; 69:67-75; PMID:24556555; http://dx.doi.org/10.1016/j.ymeth.2014.02.010
42. A.del Pozo, J.A.Sanchez-Ferez, F.J.Sanchez-Vazquez. Circadian rhythms of self-feeding and locomotor activity in zebrafish (Danio Rerio). Chronobiol Int 2011; 28:39-47; PMID:21182403; http://dx.doi.org/10.3109/07420528.2010.530728
43. S.Chung, E.J.Lee, S.Yun, H.K.Choe, S.B.Park, H.J.Son, K.S.Kim, D.E.Dluzen, I.Lee, O.Hwang, et al. Impact of circadian nuclear receptor REV-ERBalpha on midbrain dopamine production and mood regulation. Cell 2014; 157:858-68; PMID:24813609; http://dx.doi.org/10.1016/j.cell.2014.03.039
44. T.Sasaki, S.Lian, J.Qi, P.E.Bayliss, C.E.Carr, J.L.Johnson, S.Guha, P.Kobler, S.D.Catz, M.Gill, et al. Aberrant autolysosomal regulation is linked to the induction of embryonic senescence:differential roles of Beclin 1 and p53 in vertebrate Spns1 deficiency. PLoS Genetics 2014; 10:e1004409; PMID:24967584; http://dx.doi.org/10.1371/journal.pgen.1004409
45. Z.Yang, D.J.Klionsky. An overview of the molecular mechanism of autophagy. Curr Topics Microbiol Immunol 2009; 335:1-32.
46. X.Xiong, R.Tao, R.A.DePinho, X.C.Dong. The autophagy-related gene 14 (Atg14) is regulated by forkhead box O transcription factors and circadian rhythms and plays a critical role in hepatic autophagy and lipid metabolism. J Biol Chem 2012; 287:39107-14; PMID:22992773; http://dx.doi.org/10.1074/jbc.M112.412569
47. Y.Shigeyoshi, K.Taguchi, S.Yamamoto, S.Takekida, L.Yan, H.Tei, T.Moriya, S.Shibata, J.J.Loros, J.C.Dunlap, et al. Light-induced resetting of a mammalian circadian clock is associated with rapid induction of the mPer1 transcript. Cell 1997; 91:1043-53; PMID:9428526; http://dx.doi.org/10.1016/S0092-8674(00)80494-8
48. M.P.Dekens, D.Whitmore. Autonomous onset of the circadian clock in the zebrafish embryo. EMBO J 2008; 27:2757-65; PMID:18800057; http://dx.doi.org/10.1038/emboj.2008.183
49. H.Ukai, H.R.Ueda. Systems biology of mammalian circadian clocks. Ann Rev Physiol 2010; 72:579-603; http://dx.doi.org/10.1146/annurev-physiol-073109-130051
50. T.Kakizawa, S.Nishio, G.Triqueneaux, S.Bertrand, J.Rambaud, V.Laudet. Two differentially active alternative promoters control the expression of the zebrafish orphan nuclear receptor gene Rev-erbalpha. J Mol Endocrinol 2007; 38:555-68; PMID:17496157; http://dx.doi.org/10.1677/JME-06-0063
51. D.Grant, L.Yin, J.L.Collins, D.J.Parks, L.A.Orband-Miller, G.B.Wisely, S.Joshi, M.A.Lazar, T.M.Willson, W.J.Zuercher. GSK4112, a small molecule chemical probe for the cell biology of the nuclear heme receptor Rev-erbalpha. ACS Chem Biol 2010; 5:925-32; PMID:20677822; http://dx.doi.org/10.1021/cb100141y
52. I.P.Amaral, I.A.Johnston. Circadian expression of clock and putative clock-controlled genes in skeletal muscle of the zebrafish. Am J Physiol Regulatory, Integrative Comparative Physiol 2012; 302:R193-206; http://dx.doi.org/10.1152/ajpregu.00367.2011
53. J.A.Sanchez, F.J.Sanchez-Vazquez. Feeding entrainment of daily rhythms of locomotor activity and clock gene expression in zebrafish brain. Chronobiol Int 2009; 26:1120-35; PMID:19731109; http://dx.doi.org/10.3109/07420520903232092
54. S.Mai, B.Muster, J.Bereiter-Hahn, M.Jendrach. Autophagy proteins LC3B, ATG5 and ATG12 participate in quality control after mitochondrial damage and influence lifespan. Autophagy 2012; 8:47-62; PMID:22170153; http://dx.doi.org/10.4161/auto.8.1.18174
55. N.Preitner, F.Damiola, L.Lopez-Molina, J.Zakany, D.Duboule, U.Albrecht, U.Schibler. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 2002; 110:251-60; PMID:12150932; http://dx.doi.org/10.1016/S0092-8674(02)00825-5
56. Z.Gerhart-Hines, D.Feng, M.J.Emmett, L.J.Everett, E.Loro, E.R.Briggs, A.Bugge, C.Hou, C.Ferrara, P.Seale, et al. The nuclear receptor Rev-erbalpha controls circadian thermogenic plasticity. Nature 2013; 503:410-3; PMID:24162845; http://dx.doi.org/10.1038/nature12642
57. Y.Zhang, B.Fang, M.J.Emmett, M.Damle, Z.Sun, D.Feng, S.M.Armour, J.R.Remsberg, J.Jager, R.E.Soccio, et al. Discrete functions of nuclear receptor Rev-erbalpha couple metabolism to the clock. Science 2015; 348(6242):1488-92
58. K.Sakaki, S.Yoshina, X.Shen, J.Han, M.R.DeSantis, M.Xiong, S.Mitani, R.J.Kaufman. RNA surveillance is required for endoplasmic reticulum homeostasis. Proc Natl Acad Sci U S A 2012; 109:8079-84; PMID:22562797; http://dx.doi.org/10.1073/pnas.1110589109
59. C.P.Selby, A.Sancar. A cryptochrome/photolyase class of enzymes with single-stranded DNA-specific photolyase activity. Proc Natl Acad Sci U S A 2006; 103:17696-700; PMID:17062752; http://dx.doi.org/10.1073/pnas.0607993103
60. C.Guo, T.S.Tang, E.C.Friedberg. SnapShot:nucleotide excision repair. Cell 2010; 140:754-4 e1; PMID:20211143; http://dx.doi.org/10.1016/j.cell.2010.02.033
61. A.Isken, M.Golczak, V.Oberhauser, S.Hunzelmann, W.Driever, Y.Imanishi, K.Palczewski, J.von Lintig. RBP4 disrupts vitamin A uptake homeostasis in a STRA6-deficient animal model for Matthew-Wood syndrome. Cell Metab 2008; 7:258-68; PMID:18316031; http://dx.doi.org/10.1016/j.cmet.2008.01.009
62. S.G.Ahn, D.J.Thiele. Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev 2003; 17:516-28; PMID:12600944; http://dx.doi.org/10.1101/gad.1044503
63. B.Kornmann, O.Schaad, H.Bujard, J.S.Takahashi, U.Schibler. System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol 2007; 5:e34; PMID:17298173; http://dx.doi.org/10.1371/journal.pbio.0050034
64. W.Li, C.Giles, S.Li. Insights into how Spt5 functions in transcription elongation and repressing transcription coupled DNA repair. Nucleic Acids Res 2014; 42:7069-83; PMID:24813444; http://dx.doi.org/10.1093/nar/gku333
65. M.T.Lam, H.Cho, H.P.Lesch, D.Gosselin, S.Heinz, Y.Tanaka-Oishi, C.Benner, M.U.Kaikkonen, A.S.Kim, M.Kosaka, et al. Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 2013; 498:511-5; PMID:23728303; http://dx.doi.org/10.1038/nature12209
66. J.E.Gibbs, J.Blaikley, S.Beesley, L.Matthews, K.D.Simpson, S.H.Boyce, S.N.Farrow, K.J.Else, D.Singh, D.W.Ray, et al. The nuclear receptor REV-ERBalpha mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc Natl Acad Sci USA 2012; 109:582-7; PMID:22184247; http://dx.doi.org/10.1073/pnas.1106750109
67. M.S.Lee. Role of islet β cell autophagy in the pathogenesis of diabetes. Trends Endocrinol Metabol 2014; 25:620-7; http://dx.doi.org/10.1016/j.tem.2014.08.005
68. Y.Wu, A.C.Arai, G.Rumbaugh, A.K.Srivastava, G.Turner, T.Hayashi, E.Suzuki, Y.Jiang, L.Zhang, J.Rodriguez, et al. Mutations in ionotropic AMPA receptor 3 alter channel properties and are associated with moderate cognitive impairment in humans. Proc Natl Acad Sci USA 2007; 104:18163-8; PMID:17989220; http://dx.doi.org/10.1073/pnas.0708699104
69. V.Hoppmann, J.J.Wu, A.M.Soviknes, J.V.Helvik, T.S.Becker. Expression of the eight AMPA receptor subunit genes in the developing central nervous system and sensory organs of zebrafish. Dev Dynamics 2008; 237:788-99; http://dx.doi.org/10.1002/dvdy.21447
70. P.Cheng, P.Andersen, D.Hassel, B.L.Kaynak, P.Limphong, L.Juergensen, C.Kwon, D.Srivastava. Fibronectin mediates mesendodermal cell fate decisions. Development 2013; 140:2587-96; PMID:23715551 http://dx.doi.org/10.1242/dev.089052
71. D.Reyon, S.Q.Tsai, C.Khayter, J.A.Foden, J.D.Sander, J.K.Joung. FLASH assembly of TALENs for high-throughput genome editing. Nat Biotechnol 2012; 30:460-5; PMID:22484455; http://dx.doi.org/10.1038/nbt.2170
72. S.S.SmadjaStorz S, A.Tovin, P.Mracek, S.Alon, N.S.Foulkes, Y.Gothilf. Casein kinase 1delta activity:a key element in the zebrafish circadian timing system. Plos One 2013; 8:e54189; PMID:23349822; http://dx.doi.org/10.1371/journal.pone.0054189
73. P.M.Craig, T.W.Moon. Fasted zebrafish mimic genetic and physiological responses in mammals:a model for obesity and diabetes?. Zebrafish 2011; 8:109-17; PMID:21854210; http://dx.doi.org/10.1089/zeb.2011.0702
74. M.G.Grabherr, B.J.Haas, M.Yassour, J.Z.Levin, D.A.Thompson, I.Amit, X.Adiconis, L.Fan, R.Raychowdhury, Q.Zeng, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011; 29:644-52; PMID:21572440; http://dx.doi.org/10.1038/nbt.1883
75. M.D.Young, M.J.Wakefield, G.K.Smyth, A.Oshlack. Gene ontology analysis for RNA-seq:accounting for selection bias. Genome Biol 2010; 11:R14; PMID:20132535; http://dx.doi.org/10.1186/gb-2010-11-2-r14
76. M.Kanehisa, M.Araki, S.Goto, M.Hattori, M.Hirakawa, M.Itoh, T.Katayama, S.Kawashima, S.Okuda, T.Tokimatsu, et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res 2008; 36:D480-4; PMID:18077471; http://dx.doi.org/10.1093/nar/gkm882
77. B.Li, C.N.Dewey. RSEM:accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 2011; 12:323; PMID:21816040; http://dx.doi.org/10.1186/1471-2105-12-323