Browse > Article
http://dx.doi.org/10.14348/molcells.2019.2451

Drosophila CrebB is a Substrate of the Nonsense-Mediated mRNA Decay Pathway that Sustains Circadian Behaviors  

Ri, Hwajung (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST))
Lee, Jongbin (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST))
Sonn, Jun Young (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST))
Yoo, Eunseok (School of Life Sciences, Ulsan National Institute of Science and Technology (UNIST))
Lim, Chunghun (School of Life Sciences, Ulsan National Institute of Science and Technology (UNIST))
Choe, Joonho (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST))
Abstract
Post-transcriptional regulation underlies the circadian control of gene expression and animal behaviors. However, the role of mRNA surveillance via the nonsense-mediated mRNA decay (NMD) pathway in circadian rhythms remains elusive. Here, we report that Drosophila NMD pathway acts in a subset of circadian pacemaker neurons to maintain robust 24 h rhythms of free-running locomotor activity. RNA interference-mediated depletion of key NMD factors in timeless-expressing clock cells decreased the amplitude of circadian locomotor behaviors. Transgenic manipulation of the NMD pathway in clock neurons expressing a neuropeptide PIGMENT-DISPERSING FACTOR (PDF) was sufficient to dampen or lengthen free-running locomotor rhythms. Confocal imaging of a transgenic NMD reporter revealed that arrhythmic Clock mutants exhibited stronger NMD activity in PDF-expressing neurons than wild-type. We further found that hypomorphic mutations in Suppressor with morphogenetic effect on genitalia 5 (Smg5) or Smg6 impaired circadian behaviors. These NMD mutants normally developed PDF-expressing clock neurons and displayed daily oscillations in the transcript levels of core clock genes. By contrast, the loss of Smg5 or Smg6 function affected the relative transcript levels of cAMP response element-binding protein B (CrebB) in an isoform-specific manner. Moreover, the overexpression of a transcriptional repressor form of CrebB rescued free-running locomotor rhythms in Smg5-depleted flies. These data demonstrate that CrebB is a rate-limiting substrate of the genetic NMD pathway important for the behavioral output of circadian clocks in Drosophila.
Keywords
circadian rhythms; CrebB; Drosophila; nonsense-mediated mRNA decay;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Agostino, P.V., Golombek, D.A., and Meck, W.H. (2011). Unwinding the molecular basis of interval and circadian timing. Front. Integr. Neurosci., 5, 64.   DOI
2 Allada, R., White, N.E., So, W.V., Hall, J.C., and Rosbash, M. (1998). A mutant Drosophila homolog of mammalian clock disrupts circadian rhythms and transcription of period and timeless. Cell 93, 791-804.   DOI
3 Alonso, C.R. (2005). Nonsense-mediated RNA decay: a molecular system micromanaging individual gene activities and suppressing genomic noise. Bioessays 27, 463-466.   DOI
4 Aronson, B.D., Johnson, K.A., Loros, J.J., and Dunlap, J.C. (1994). Negative feedback defining a circadian clock: autoregulation of the clock gene frequency. Science 263, 1578-1584.   DOI
5 Avery, P., Vicente-Crespo, M., Francis, D., Nashchekina, O., Alonso, C. R., and Palacios, I.M. (2011). Drosophila Upf1 and Upf2 loss of function inhibits cell growth and causes animal death in a Upf3-independent manner. RNA 17, 624-638.   DOI
6 Barberan-Soler, S., and Zahler, A.M. (2008). Alternative splicing regulation during C. elegans development: splicing factors as regulated targets. PLoS Genet. 4, e1000001.   DOI
7 Lim, C., and Allada, R. (2013). Emerging roles for post-transcriptional regulation in circadian clocks. Nat. Neurosci. 16, 1544-1550.   DOI
8 Lim, C., Chung, B.Y., Pitman, J.L., McGill, J.J., Pradhan, S., Lee, J., Allada, R. (2007). Clockwork orange encodes a transcriptional repressor important for circadian-clock amplitude in Drosophila. Curr. Biol. 17, 1082-1089.   DOI
9 Lim, C., Lee, J., Choi, C., Kilman, V.L., Kim, J., Park, S.M., Jang S.K., Allada R. and Choe, J. (2011). The novel gene twenty-four defines a critical translational step in the Drosophila clock. Nature 470, 399-403.   DOI
10 Lim, C., Lee, J., Choi, C., Kim, J., Doh, E., and Choe, J. (2007). Functional role of CREB-binding protein in the circadian clock system of Drosophila melanogaster. Mol. Cell. Biol. 27, 4876-4890.   DOI
11 Lin, Y., Stormo, G.D., and Taghert, P.H. (2004). The neuropeptide pigment-dispersing factor coordinates pacemaker interactions in the Drosophila circadian system. J. Neurosci. 24, 7951-7957.   DOI
12 Sun, X., Dang, F., Zhang, D., Yuan, Y., Zhang, C., Wu, Y., Wang, Y. and Liu, Y. (2015). Glucagon-CREB/CRTC2 signaling cascade regulates hepatic BMAL1 protein. J. Biol. Chem. 290, 2189-2197.   DOI
13 Shimizu, F., and Fukada, Y. (2007). Circadian phosphorylation of ATF-2, a potential activator of Period2 gene transcription in the chick pineal gland. J. Neurochem. 103, 1834-1842.   DOI
14 Stanewsky, R., Kaneko, M., Emery, P., Beretta, B., Wager-Smith, K., Kay, S.A., Rosbash, M., and Hall, J.C. (1998). The cry(b) mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95, 681-692.   DOI
15 Stoleru, D., Peng, Y., Agosto, J., and Rosbash, M. (2004). Coupled oscillators control morning and evening locomotor behaviour of Drosophila. Nature 431, 862-868.   DOI
16 Suri, V., Lanjuin, A., and Rosbash, M. (1999). TIMELESS-dependent positive and negative autoregulation in the Drosophila circadian clock. Embo J. 18, 675-686.   DOI
17 Tabrez, S.S., Sharma, R.D., Jain, V., Siddiqui, A.A., and Mukhopadhyay, A. (2017). Differential alternative splicing coupled to nonsense-mediated decay of mRNA ensures dietary restriction-induced longevity. Nat. Commun. 8, 306.   DOI
18 Matsumoto, A., Ukai-Tadenuma, M., Yamada, R.G., Houl, J., Uno, K.D., Kasukawa, T., Dauwalder, B., Itoh, T.Q., Takahashi, K., Ueda, R., et al. (2007). A functional genomics strategy reveals clockwork orange as a transcriptional regulator in the Drosophila circadian clock. Genes Dev. 21, 1687-1700.   DOI
19 Beckwith, E.J., and Ceriani, M.F. (2015). Experimental assessment of the network properties of the Drosophila circadian clock. J. Comp. Neurol. 523, 982-996.   DOI
20 Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.   DOI
21 Maurer, C., Winter, T., Chen, S.W., Hung, H.C., and Weber, F. (2016). The CREB-binding protein affects the circadian regulation of behaviour. FEBS Lett. 590, 3213-3220.   DOI
22 Behm-Ansmant, I., Kashima, I., Rehwinkel, J., Sauliere, J., Wittkopp, N., and Izaurralde, E. (2007). mRNA quality control: an ancient machinery recognizes and degrades mRNAs with nonsense codons. FEBS Lett. 581, 2845-2853.   DOI
23 Belvin, M.P., Zhou, H., and Yin, J.C. (1999). The Drosophila dCREB2 gene affects the circadian clock. Neuron 22, 777-787.   DOI
24 Blau, J., and Young, M.W. (1999). Cycling vrille expression is required for a functional Drosophila clock. Cell 99, 661-671.   DOI
25 Brunner, M., and Schafmeier, T. (2006). Transcriptional and post-transcriptional regulation of the circadian clock of cyanobacteria and Neurospora. Genes Dev. 20, 1061-1074.   DOI
26 Chan, W.K., Huang, L., Gudikote, J.P., Chang, Y.F., Imam, J.S., MacLean, J.A. 2nd, and Wilkinson, M.F. (2007). An alternative branch of the nonsense-mediated decay pathway. Embo. J. 26, 1820-1830.   DOI
27 Chang, Y.F., Imam, J.S., and Wilkinson, M.F. (2007). The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 76, 51-74.   DOI
28 Chapin, A., Hu, H., Rynearson, S.G., Hollien, J., Yandell, M., and Metzstein, M.M. (2014). In vivo determination of direct targets of the nonsense-mediated decay pathway in Drosophila. G3 (Bethesda) 4, 485-496.   DOI
29 Cheng, P., Yang, Y.H., and Liu, Y. (2001). Interlocked feedback loops contribute to the robustness of the Neurospora circadian clock. Proc. Natl. Acad. Sci. USA 98, 7408-7413.   DOI
30 Mendell, J.T., Sharifi, N.A., Meyers, J.L., Martinez-Murillo, F.M., and Dietz, H.C. (2004). Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise. Nat. Genet. 36, 1073-1078.   DOI
31 Merrow, M., Franchi, L., Dragovic, Z., Gorl, M., Johnson, J., Brunner, M., Macino, G., and Roenneberg, T. (2001). Circadian regulation of the light input pathway in Neurospora crassa. Embo J., 20, 307-315.   DOI
32 Metzstein, M.M., and Krasnow, M.A. (2006). Functions of the nonsense-mediated mRNA decay pathway in Drosophila development. PLoS Genet 2, e180.   DOI
33 Micale, L., Muscarella, L.A., Marzulli, M., Augello, B., Tritto, P., D'Agruma, L., Zelante, L., Palumbo, G., and Merla, G. (2009). VHL frameshift mutation as target of nonsense-mediated mRNA decay in Drosophila melanogaster and human HEK293 cell line. J. Biomed. Biotechnol. 2009, 860761.
34 Morgan, L.W., and Feldman, J.F. (1997). Isolation and characterization of a temperature-sensitive circadian clock mutant of Neurospora crassa. Genetics 146, 525-530.   DOI
35 Muhlemann, O. (2008). Recognition of nonsense mRNA: towards a unified model. Biochem. Soc. Trans 36, 497-501.   DOI
36 Vosshall, L.B., Price, J.L., Sehgal, A., Saez, L., and Young, M.W. (1994). Block in nuclear localization of period protein by a second clock mutation, timeless. Science 263, 1606-1609.   DOI
37 O'Neill, J.S., Maywood, E.S., Chesham, J.E., Takahashi, J.S., and Hastings, M.H. (2008). cAMP-dependent signaling as a core component of the mammalian circadian pacemaker. Science 320, 949-953.   DOI
38 Traunmuller, L., Bornmann, C., and Scheiffele, P. (2014). Alternative splicing coupled nonsense-mediated decay generates neuronal cell type-specific expression of SLM proteins. J. Neurosci. 34, 16755-16761.   DOI
39 Travnickova-Bendova, Z., Cermakian, N., Reppert, S.M., and Sassone-Corsi, P. (2002). Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity. Proc. Natl. Acad. Sci. USA 99, 7728-7733.   DOI
40 Tubon, T.C., Jr., Zhang, J., Friedman, E.L., Jin, H., Gonzales, E.D., Zhou, H., Drier, D., Gerstner, J.R., Paulson, E.A., Fropf, R., et al. (2013). dCREB2-mediated enhancement of memory formation. J. Neurosci. 33, 7475-7487.   DOI
41 Williams, J.A., Su, H.S., Bernards, A., Field, J., and Sehgal, A. (2001). A circadian output in Drosophila mediated by neurofibromatosis-1 and Ras/MAPK. Science 293, 2251-2256.   DOI
42 Wu, Y., Zhang, Y., Sun, Y., Yu, J., Wang, P., Ma, H., Chen, S., Ma, L., Zhang, D., He, Q., et al. (2017). Up-frameshift protein UPF1 regulates neurospora crassa circadian and diurnal growth rhythms. Genetics 206, 1881-1893   DOI
43 Yepiskoposyan, H., Aeschimann, F., Nilsson, D., Okoniewski, M., and Muhlemann, O. (2011). Autoregulation of the nonsense-mediated mRNA decay pathway in human cells. RNA 17, 2108-2118.   DOI
44 Depetris-Chauvin, A., Berni, J., Aranovich, E.J., Muraro, N.I., Beckwith, E.J., and Ceriani, M.F. (2011). Adult-specific electrical silencing of pacemaker neurons uncouples molecular clock from circadian outputs. Curr. Biol. 21, 1783-1793.   DOI
45 Cyran, S.A., Buchsbaum, A.M., Reddy, K.L., Lin, M.C., Glossop, N.R., Hardin, P.E., Young M.W., Storti R.V., and Blau, J. (2003). vrille, Pdp1, and dClock form a second feedback loop in the Drosophila circadian clock. Cell 112, 329-341.   DOI
46 Davis, G.W., Schuster, C.M., and Goodman, C.S. (1996). Genetic dissection of structural and functional components of synaptic plasticity. III. CREB is necessary for presynaptic functional plasticity. Neuron 17, 669-679.   DOI
47 Decker, C.J., and Parker, R. (2012). P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harb. Perspect. Biol. 4, a012286.   DOI
48 Eckel-Mahan, K.L., Phan, T., Han, S., Wang, H., Chan, G.C., Scheiner, Z.S., and Storm, D.R. (2008). Circadian oscillation of hippocampal MAPK activity and cAmp: implications for memory persistence. Nat. Neurosci. 11, 1074-1082.   DOI
49 Emery, P., So, W.V., Kaneko, M., Hall, J.C., and Rosbash, M. (1998). CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95, 669-679.   DOI
50 Eulalio, A., Behm-Ansmant, I., and Izaurralde, E. (2007). P bodies: at the crossroads of post-transcriptional pathways. Nat. Rev. Mol. Cell Biol. 8, 9-22.   DOI
51 Filichkin, S.A., Cumbie, J.S., Dharmawadhana, J.P., Jaiswal, P., Chang, J.H., Palusa, S.G., Reddy A.S., Megraw, M., and Mockler, T.C., (2015). Environmental stresses modulate abundance and timing of alternatively spliced circadian transcripts in Arabidopsis. Mol. Plant 8, 207-227.   DOI
52 Peng, Y., Stoleru, D., Levine, J.D., Hall, J.C., and Rosbash, M. (2003). Drosophila free-running rhythms require intercellular communication. PLoS Biol. 1, E13.   DOI
53 Obrietan, K., Impey, S., Smith, D., Athos, J., and Storm, D.R. (1999). Circadian regulation of cAMP response element-mediated gene expression in the suprachiasmatic nuclei. J. Biol. Chem. 274, 17748-17756.   DOI
54 Palacios-Munoz, A., and Ewer, J. (2018). Calcium and cAMP directly modulate the speed of the Drosophila circadian clock. PLoS Genet. 14, e1007433.   DOI
55 Park, S., Sonn, J.Y., Oh, Y., Lim, C., and Choe, J. (2014). SIFamide and SIFamide receptor defines a novel neuropeptide signaling to promote sleep in Drosophila. Mol. Cells 37, 295-301.   DOI
56 Perazzona, B., Isabel, G., Preat, T., and Davis, R.L. (2004). The role of cAMP response element-binding protein in Drosophila long-term memory. J. Neurosci. 24, 8823-8828.   DOI
57 Peschel, N., and Helfrich-Forster, C. (2011). Setting the clock-by nature: circadian rhythm in the fruitfly Drosophila melanogaster. FEBS Lett. 585, 1435-1442.   DOI
58 Pfeiffenberger, C., Lear, B.C., Keegan, K.P., and Allada, R. (2010). Processing circadian data collected from the Drosophila activity monitoring (DAM) system. Cold Spring Harb. Protoc. 2010, pdb prot5519.
59 Nickless, A., Bailis, J.M., and You, Z. (2017). Control of gene expression through the nonsense-mediated RNA decay pathway. Cell Biosci. 7, 26.   DOI
60 Yin, J.C., Del Vecchio, M., Zhou, H., and Tully, T. (1995). CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81, 107-115.   DOI
61 Ginty, D.D., Kornhauser, J.M., Thompson, M.A., Bading, H., Mayo, K. E., Takahashi, J.S., and Greenberg, M.E. (1993). Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 260, 238-241.   DOI
62 Frizzell, K.A., Rynearson, S.G., and Metzstein, M.M. (2012). Drosophila mutants show NMD pathway activity is reduced, but not eliminated, in the absence of Smg6. RNA 18, 1475-1486.   DOI
63 Fropf, R., Tubon, T.C., Jr., and Yin, J.C. (2013). Nuclear gating of a Drosophila dCREB2 activator is involved in memory formation. Neurobiol. Learn Mem. 106, 258-267.   DOI
64 Fukuhara, C., Liu, C., Ivanova, T.N., Chan, G.C., Storm, D.R., Iuvone, P.M., and Tosini, G. (2004). Gating of the cAMP signaling cascade and melatonin synthesis by the circadian clock in mammalian retina. J. Neurosci. 24, 1803-1811.   DOI
65 Grima, B., Chelot, E., Xia, R.H., and Rouyer, F. (2004). Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431, 869-873.   DOI
66 Hatano, M., Umemura, M., Kimura, N., Yamazaki, T., Takeda, H., Nakano, H., Takahashi, S., Takahashi, Y. (2013). The 5'-untranslated region regulates ATF5 mRNA stability via nonsense-mediated mRNA decay in response to environmental stress. FEBS J. 280, 4693-4707.   DOI
67 Hendricks, J.C., Williams, J.A., Panckeri, K., Kirk, D., Tello, M., Yin, J.C., and Sehgal, A. (2001). A non-circadian role for cAMP signaling and CREB activity in Drosophila rest homeostasis. Nat. Neurosci. 4, 1108-1115.   DOI
68 Hosoda, H., Kato, K., Asano, H., Ito, M., Kato, H., Iwamoto, Suzuki, A., Masushige, S., and Kida, S. (2009). CBP/p300 is a cell type-specific modulator of CLOCK/BMAL1-mediated transcription. Mol. Brain 2, 34.   DOI
69 Hug, N., Longman, D., and Caceres, J.F. (2016). Mechanism and regulation of the nonsense-mediated decay pathway. Nucleic Acids Res. 44, 1483-1495.   DOI
70 Price, J.L., Dembinska, M.E., Young, M.W., and Rosbash, M. (1995). Suppression of PERIOD protein abundance and circadian cycling by the Drosophila clock mutation timeless. Embo J. 14, 4044-4049.   DOI
71 Popp, M.W., and Maquat, L.E. (2014). The dharma of nonsense-mediated mRNA decay in mammalian cells. Mol. Cells 37, 1-8.   DOI
72 Richier, B., Michard-Vanhee, C., Lamouroux, A., Papin, C., and Rouyer, F. (2008). The clockwork orange Drosophila protein functions as both an activator and a repressor of clock gene expression. J. Biol. Rhythms. 23, 103-116.   DOI
73 Rutila, J.E., Suri, V., Le, M., So, W.V., Rosbash, M., and Hall, J.C. (1998). CYCLE is a second bHLH-PAS clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell 93, 805-814.   DOI
74 Sakamoto, K., Norona, F.E., Alzate-Correa, D., Scarberry, D., Hoyt, K. R., and Obrietan, K. (2013). Clock and light regulation of the CREB coactivator CRTC1 in the suprachiasmatic circadian clock. J. Neurosci. 33, 9021-9027.   DOI
75 Zheng, D., Chen, C.Y., and Shyu, A.B. (2011). Unraveling regulation and new components of human P-bodies through a protein interaction framework and experimental validation. RNA 17, 1619-1634.   DOI
76 Yin, J.C., Wallach, J.S., Del Vecchio, M., Wilder, E.L., Zhou, H., Quinn, W.G., and Tully, T. (1994). Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79, 49-58.   DOI
77 Yin, J.C., Wallach, J.S., Wilder, E.L., Klingensmith, J., Dang, D., Perrimon, N., Zhou, H., Tully, T., and. Quinn, W.G. (1995). A Drosophila CREB/CREM homolog encodes multiple isoforms, including a cyclic AMP-dependent protein kinase-responsive transcriptional activator and antagonist. Mol. Cell. Biol. 15, 5123-5130.   DOI
78 Yu, D., Akalal, D.B., and Davis, R.L. (2006). Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. Neuron 52, 845-855.   DOI
79 Zhou, J., Yu, W., and Hardin, P.E. (2016). Clockwork orange enhances period mediated rhythms in transcriptional repression by antagonizing E-box binding by clock-cycle. PLoS Genet 12, e1006430.   DOI
80 Scheving, L.A., and Gardner, W. (1998). Circadian regulation of CREB transcription factor in mouse esophagus. Am. J. Physiol. 274, C1011-1016.   DOI
81 Schoning, J.C., Streitner, C., Meyer, I.M., Gao, Y., and Staiger, D. (2008). Reciprocal regulation of glycine-rich RNA-binding proteins via an interlocked feedback loop coupling alternative splicing to nonsense-mediated decay in Arabidopsis. Nucleic Acids Res. 36, 6977-6987.   DOI
82 Schoning, J.C., Streitner, C., Page, D.R., Hennig, S., Uchida, K., Wolf, E., Furuya, M. and Staiger, D. (2007). Auto-regulation of the circadian slave oscillator component AtGRP7 and regulation of its targets is impaired by a single RNA recognition motif point mutation. Plant J. 52(6), 1119-1130.   DOI
83 Kako, K., Wakamatsu, H., and Ishida, N. (1996). c-fos CRE-binding activity of CREB/ATF family in the SCN is regulated by light but not a circadian clock. Neurosci. Lett. 216, 159-162.   DOI
84 Hung, H.C., Maurer, C., Kay, S.A., and Weber, F. (2007). Circadian transcription depends on limiting amounts of the transcription co-activator nejire/CBP. J. Biol. Chem. 282, 31349-31357.   DOI
85 Johansson, M.J., He, F., Spatrick, P., Li, C., and Jacobson, A. (2007). Association of yeast Upf1p with direct substrates of the NMD pathway. Proc. Natl. Acad. Sci. USA 104, 20872-20877.   DOI
86 Kadener, S., Stoleru, D., McDonald, M., Nawathean, P., and Rosbash, M. (2007). Clockwork orange is a transcriptional repressor and a new Drosophila circadian pacemaker component. Genes Dev. 21, 1675-1686.   DOI
87 Kim, M., Lee, H., Hur, J.H., Choe, J., and Lim, C. (2016). CRTC Potentiates light-independent timeless transcription to sustain circadian rhythms in Drosophila. Sci. Rep. 6, 32113.   DOI
88 Kojima, S., Shingle, D.L., and Green, C.B. (2011). Post-transcriptional control of circadian rhythms. J. Cell Sci. 124, 311-320.   DOI
89 Konopka, R.J., and Benzer, S. (1971). Clock mutants of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 68, 2112-2116.   DOI
90 Koyanagi, S., Hamdan, A.M., Horiguchi, M., Kusunose, N., Okamoto, A., Matsunaga, N., and Ohdo, S. (2011). cAMP-response element (CRE)-mediated transcription by activating transcription factor-4 (ATF4) is essential for circadian expression of the Period2 gene. J. Biol. Chem. 286, 32416-32423.   DOI
91 Kwon, Y.J., Park, M.J., Kim, S.G., Baldwin, I.T., and Park, C.M. (2014). Alternative splicing and nonsense-mediated decay of circadian clock genes under environmental stress conditions in Arabidopsis. BMC Plant. Biol. 14, 136.   DOI
92 Lewis, B.P., Green, R.E., and Brenner, S.E. (2003). Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proc. Natl. Acad. Sci. USA 100, 189-192.   DOI
93 Lee, B., Li, A., Hansen, K.F., Cao, R., Yoon, J.H., and Obrietan, K. (2010). CREB influences timing and entrainment of the SCN circadian clock. J. Biol. Rhythms. 25, 410-420.   DOI
94 Lee, Y., Lee, J., Kwon, I., Nakajima, Y., Ohmiya, Y., Son, G.H., Lee, K.H., and Kim, K. (2010). Coactivation of the CLOCK-BMAL1 complex by CBP mediates resetting of the circadian clock. J. Cell Sci. 123, 3547-3557.   DOI
95 Lemos, D.R., Goodspeed, L., Tonelli, L., Antoch, M.P., Ojeda, S.R., and Urbanski, H.F. (2007). Evidence for circadian regulation of activating transcription factor 5 but not tyrosine hydroxylase by the chromaffin cell clock. Endocrinology 148, 5811-5821.   DOI
96 Shen, Y., Wu, X., Liu, D., Song, S., Liu, D., and Wang, H. (2016). Cold-dependent alternative splicing of a Jumonji C domain-containing gene MtJMJC5 in Medicago truncatula. Biochem. Biophys. Res. Commun. 474, 271-276.   DOI
97 Sehgal, A., Price, J.L., Man, B., and Young, M.W. (1994). Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science 263, 1603-1606.   DOI
98 Shaul, O. (2015). Unique aspects of plant nonsense-mediated mRNA decay. Trends Plant Sci. 20, 767-779.   DOI